You are on page 1of 11

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/271904519

Postmortem Biochemical and Microbiological Changes in Loricariid Catfish


(Pterygoplichthys disjunctivus) Muscle During Ice Storage

Article  in  Journal of Aquatic Food Product Technology · November 2015


DOI: 10.1080/10498850.2013.828146

CITATION READS

1 320

7 authors, including:

Enrique Marquez Rios Ramon Pacheco-Aguilar


Universidad de Sonora (Unison) Research Center for Food and Development A.C.
120 PUBLICATIONS   981 CITATIONS    102 PUBLICATIONS   1,942 CITATIONS   

SEE PROFILE SEE PROFILE

Juan Carlos Ramírez-Suárez Víctor Manuel Ocaño-Higuera


Research Center for Food and Development A.C. Universidad de Sonora (Unison)
66 PUBLICATIONS   909 CITATIONS    48 PUBLICATIONS   588 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Biotecnia View project

Collaborations View project

All content following this page was uploaded by Enrique Marquez Rios on 18 April 2016.

The user has requested enhancement of the downloaded file.


Journal of Aquatic Food Product Technology

ISSN: 1049-8850 (Print) 1547-0636 (Online) Journal homepage: http://www.tandfonline.com/loi/wafp20

Postmortem Biochemical and Microbiological


Changes in Loricariid Catfish (Pterygoplichthys
disjunctivus) Muscle During Ice Storage

Enrique Marquez-Rios, Ramon Pacheco-Aguilar, Juan Carlos Ramirez-Suarez,


Victor M. Ocano-Higuera, Celia O. García-Sifuentes, Susana M. Scheuren-
Acevedo & Miguel A. Mazorra-Manzano

To cite this article: Enrique Marquez-Rios, Ramon Pacheco-Aguilar, Juan Carlos Ramirez-
Suarez, Victor M. Ocano-Higuera, Celia O. García-Sifuentes, Susana M. Scheuren-Acevedo &
Miguel A. Mazorra-Manzano (2016) Postmortem Biochemical and Microbiological Changes in
Loricariid Catfish (Pterygoplichthys disjunctivus) Muscle During Ice Storage, Journal of Aquatic
Food Product Technology, 25:1, 105-113, DOI: 10.1080/10498850.2013.828146

To link to this article: http://dx.doi.org/10.1080/10498850.2013.828146

Accepted author version posted online: 21


Aug 2014.
Published online: 21 Aug 2016.

Submit your article to this journal

Article views: 28

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at


http://www.tandfonline.com/action/journalInformation?journalCode=wafp20

Download by: [University of Sonora], [E. Marquez-Rios] Date: 22 January 2016, At: 08:30
JOURNAL OF AQUATIC FOOD PRODUCT TECHNOLOGY
2016, VOL. 25, NO. 1, 105–113
http://dx.doi.org/10.1080/10498850.2013.828146

Postmortem Biochemical and Microbiological Changes in


Loricariid Catfish (Pterygoplichthys disjunctivus) Muscle During Ice
Storage
Enrique Marquez-Riosa, Ramon Pacheco-Aguilara, Juan Carlos Ramirez-Suareza,
Victor M. Ocano-Higuerab, Celia O. García-Sifuentesa, Susana M. Scheuren-Acevedoa,
and Miguel A. Mazorra-Manzanoa
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

a
Research Center for Food and Development, Hermosillo, Sonora, Mexico; bDepartment of Chemical and Biological
Sciences, University of Sonora, Hermosillo, Sonora, México

ABSTRACT KEY WORDS


Postmortem biochemical and microbiological changes in loricariid catfish loricariid catfish;
(Pterygoplichthys disjunctivus) muscle were evaluated during ice storage for Pterygoplichthys disjunctivus;
20 days. Values of pH remained stable for 15 days (7.4 ± 0.2), and total postmortem muscle
volatile base-nitrogen (TVB-N) remained under acceptable limits throughout changes; K-value;
microbiological changes
storage, with a final value of 25.2 ± 3.3 mg N/100 g muscle at Day 20.
Adenosine-5´-triphosphate (ATP) and derivatives followed a postmortem
degradation pattern similar to other species, with the K-value being the
best freshness loss indicator. Biochemical and microbiological changes
indicated that the shelf life of iced loricariid catfish muscle was 15 days
under optimal (0°C) storage conditions.

Introduction
The world apparent consumption of fish and its products has increased in the last years, with a per
capita consumption of 17 kg/year in 2007 and an increase of 3.6%/year since 1996 (Food and
Agriculture Organization of the United Nations [FAO], 2011). Even though the world capture of fish
has stabilized in the last 10 years, the increase in its demand has been satisfied in part due to
aquaculture practices and the use of nontraditional species (Jiang, 2010). The evaluation of new
species for human consumption depends on several characteristics—including availability, size and
yield, technological value, and nutritional and sensorial quality. In addition to its nutritive value, fish
products offer a high potential of novel healthy food ingredients and biologically active compounds
still unknown for most species. In addition, the major factors that govern the use of potential
nontraditional species for direct and indirect human consumption are poorly identified.
The loricariid catfish Pterygoplichthys disjunctivus (Siluriformes: Loricariidae; Weber, 1991) is
endemic to South America (except Chile), Panamá, and Costa Rica (Armbruster and Page, 2006). It
is an ornamental fish commonly used in North America and other parts of the world to clean fish
tanks from algae and other debris. However, the species has made it through to the wild and invaded
different water corps throughout the world. Such is the case of México, where some species have
accidentally invaded dams and rivers causing some ecological problems that have impacted some
local fisheries. One example is the invasion of the Adolfo Lopez Mateos dam (aka “El Infiernillo”) in
the State of Michoacán, México, affecting the economy of the surrounding fisheries communities
(Mendoza et al., 2009), who depend on the Balsas catfish (Ictalurus balsanus), the redside cichlid
(Cichlasoma istlanum), and tilapia fisheries. The loricariid catfish, besides causing problems with the

CONTACT Juan Carlos Ramírez-Suarez jcramirez@ciad.mx Centro de Investigación en Alimentación y Desarrollo, A.C.
Carretera a La Victoria, Km. 0.6., P.O. Box 1735, Hermosillo, Sonora, 83000, México
© 2016 Taylor & Francis
106 E. MARQUEZ-RIOS ET AL.

fishermen’s nets, somehow has affected the rest of the fisheries. By 2010, its stock was estimated as
100,000 tons and growing fast (Martínez-Palacios et al., 2010).
One wise way of controlling the loricariid catfish population is by exploiting this resource.
However, the quality, usefulness, and technological value depend on the species, fishing conditions,
and biochemical changes occurring during storage conditions after the fish death, which in turn are
dependent on endogenous enzymes, microbial contamination, and postcatch handling.
The biochemical changes that cause loss of freshness generally occur before the fish is spoiled by
bacterial and enzymatic action (Ehira and Uchiyama, 1973). The knowledge of most physicochem-
ical, biochemical, and microbiological changes occurring under optimum postcatch handling and ice
storage (0°C) is a valuable tool for fish postharvest management and processing. Any deviation—
such as improper handling, contamination, or temperature abuse—has a detrimental effect on its life
time storage.
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

Although the species has been recently used for food purposes by locals, a fundamental research
on biochemical postmortem and microbiological changes occurring in loricariid catfish is necessary.
Defining the quality parameters for the species could help fishermen and processors in establishing
better processing and marketing strategies, turning a problem in opportunity. Hence, the objective of
the present study was to elucidate the postmortem biochemical and microbiological changes
occurring in muscle of the loricariid catfish (P. disjunctivus) during ice storage.

Materials and methods


Raw material
Loricariid catfish (P. disjunctivus) was harvested from “El Infiernillo” dam (Michoacán, Mexico)
using a gillnet method. A batch of 35 specimens was obtained during October 2009. Specimens
collected were immediately set on ice coolers in alternated layers of fish-ice and transported to the
Aquaculture Laboratory of the Universidad Michoacana de San Nicolás de Hidalgo in Morelia,
Michoacán, México. Fish was gutted, and the body muscle section was cut (leaving backbone and
skin on), washed with water, placed in Ziploc® (S. C. Johnson & Son, Inc., Racine, WI, USA) frozen
bags, and set in a cooler in alternating layers of bagged fish and ice and transported to the Seafood
Laboratory at the Centro de Investigación en Alimentación y Desarrollo in Hermosillo, Sonora,
Mexico. Samples reached this last lab 24 h after sampling. There, the bagged loricariid catfish muscle
was subjected to 20 days of ice storage in the same cooler, with ice exchanges every 2 days. Five
specimens were sampled (n = 5) at Days 1, 3, 5, 8, 11, 15, and 20 of ice storage.
Samples used for physicochemical (proximate composition, total volatile base nitrogen [TVB-N],
pH, and color) and biochemical (adenosine-5´-triphosphate [ATP] and related compounds) analysis
were frozen at −86°C, while the ones used for microbiological analyses were monitored in fresh. All
analytical determinations were carried out in duplicate. Each individual muscle was manually
filleted, removing backbone and skin, and homogenized in a Cuisinart DCl 8 food processor
(Cuisinart Inc., Greenwich, CT, USA). All analyses (except color) were carried out on the homo-
genized sample.

Physicochemical analyses
Proximate composition (moisture, ash, fat, and protein) was determined following the AOAC (1993;
Methods 950.46, 938.08, 960.39, and 955.04, respectively). Extracts for nonprotein nitrogen (NPN)
were prepared by homogenizing 50 g of minced fish with 100 mL of 10% trichloroacetic acid (TCA)
solution in a blender for 2 min. The homogenate was filtered through #1 Whatman paper and NPN
determined by micro-Kjeldahl method (Method 955.04) of AOAC (1993). Total volatile base
nitrogen (TVB-N) and pH were measured according to Woyewoda et al. (1986). Color was measured
on fillets (before homogenization) using a Konica-Minolta CR-400 Tristimulus Colorimeter (Konica
JOURNAL OF AQUATIC FOOD PRODUCT TECHNOLOGY 107

Minolta Sensing, Inc., Tokyo, Japan). Color coordinates were used to measure the degree of lightness
(L*), redness-greenness (+ or − a*), and yellowness-blueness (+ or − b*). For a better integration and
interpretation of a* and b* values, hue angles (θ) were calculated using the formula:
θ ¼ Arctanðb =a Þ:
Also, chromaticity was calculated using the formula:
 1=2
C ¼ ða Þ2 þ ðb Þ2 :

Biochemical analysis
Nucleotides and related compounds analyses were carried out by reverse phase high performance
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

liquid chromatography (Ryder, 1985). Identification of nucleotides, nucleosides, and bases was made
by comparing their retention times with those from commercial standards of ATP, adenosine-5
´-diphosphate (ADP), adenosine-5´-monophosphate (AMP), inosine-5´-monophosphate (IMP),
inosine (HxR), and hypoxantine (Hx; Sigma Chemicals Co., St. Louis, MO, USA). From the results,
the K and Ki values (%) were calculated as follows:
%K ¼ ½ðHxR þ HxÞ=ðATP þ ADP þ AMP þ IMP þ HxR þ HxÞ  100; (1)

%Ki ¼ ½ðHxR þ HxÞ=ðIMP þ HxR þ HxÞ  100: (2)

Microbiological analysis
Microbiological analyses were carried out in fresh muscle (10 g) according to the U.S. Food and
Drug Administration’s (FDA) Bacteriological Analytical Manual. Total plate count (TPC; Maturin
and Peeler, 2001) was evaluated for aerobic mesophilic and psychrophilic microorganisms (CFU g−1)
using plate count agar and incubating at 35 ± 1 and 5 ± 2°C, respectively. Total and fecal coliforms
(MPN) were evaluated using bile crystal violet neutral red agar with addition of superficial virgin oil
layer at 35–37°C for 24 h (Baygar et al., 2008). The presence of bacterial pathogens such as
Staphylococcus aureus (on Baird Parker agar at 35–37°C; Bennet and Lancette, 2001), Salmonella
spp. (preenriched with buffered peptonated water followed by selective enrichment with selenite
cystine broth and tetrathionate-bright green broth and isolated with bismuth sulphite agar and
bright green red-phenol agar at 35–37°C; Andrews et al., 2011), and Vibrio spp. (on alkaline peptone
water and thiosulphate citrate bile salts at 35–37°C; Kaysner and DePaola, 2004) were evaluated.

Statistical analysis
All analytical determinations were carried out in duplicate. Descriptive statistics (mean, standard
deviation, and variation coefficient), one-way analysis of variance (ANOVA), multiple comparison
by the Tukey test, and linear regression analysis were applied. A significance level of 5% was used.

Results and discussion


Physical characteristic and proximate analysis
Loricariid catfish (P. disjunctivus) showed an average weight and length (n = 20) of 157.3 ± 64.1 g
and 20.1 ± 3.1 cm, respectively, and a muscle yield of 16.6 ± 1.5%. This low yield is due to its
physiological characteristics since it possesses a higher viscera content (> 10% of the total body
weight versus 5% of most fish) than regular fish (Villalba-Villalba et al., 2011), thicker skin, and large
fins, among others parameters.
108 E. MARQUEZ-RIOS ET AL.

Loricariid catfish muscle proximate composition resulted as follows: 81.8 ± 0.2% moisture, 17.5 ±
0.5% protein, 0.7 ± 0.1% lipids, 1.0 ± 0.1% ash, and 0.02 ± 0.0% NPN. This muscle proximate
composition (high protein and low fat contents) is in agreement with white lean fleshed fish
(Pacheco-Aguilar et al., 2003), such as cod (Gadus morhua callaries), a lean fish from the Baltic
area (Usydus et al., 2011); these characteristics place the Loricariid catfish in the category of lean fish,
with a good source of protein. However, its muscle appearance is similar to fatty fish with some
amount of dark muscle.

pH and TVB-N
Even though the pH of live marine fish muscle is usually close to 7, the postmortem muscle pH can
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

vary depending on season, species, muscle components, buffering capacity of muscle proteins, and
other factors (Church, 1998). In this study, the loricariid catfish postmortem muscle pH varied (p ≥
0.05) from an initial value (Day 1) of 7.5 ± 0.3 to 8.2 ± 0.5 at the end of the ice storage period
(Figure 1). This initial high pH is most probably due to its habitat, where high pH conditions (from
7 to 8) are found (CONANP, 2006). The pH remained stable (p ≥ 0.05) for the first 15 days of ice
storage (0°C), then an increase (p ≥ 0.05) was observed. Even though muscular pH usually tends to
decrease during the first hours postmortem, mainly as a result of lactic acid and ATP metabolites
accumulation, its behavior greatly depends on the buffering capacity of muscle proteins which, at the
same time, depends on the species or biological condition of fish. Since no pH variation was
observed during the first storage days in the present study, this can be an indication of the good
buffering capacity of this type of muscle (Ogata, 2002).
The high pH shown at the end of the storage days (0°C) could be due to alkaline metabolites
produced from the increasing bacterial accumulation (see Microbiological Analysis section). Similar
results were found by Chomnawang et al. (2007), who reported a gradual increase in pH of hybrid
catfish (Clarias macrocephalus × Clarias gariepinus) stored at 4°C.
A chemical parameter that is commonly used to evaluate fish muscle spoilage (quality) is TVB-N.
Figure 1 shows a steady behavior for TVB-N values (p ≥ 0.05) during muscle storage on ice (0°C),
with values ranging from 24.9 ± 2.7 (Day 1) to 25.2 ± 3.3 (Day 20) mg N/100 g muscle during the

9.0 30
TVB-N (mg N/100g muscle)

8.5
25
8.0
pH

7.5 20

7.0
pH
TVB 15
6.5

6.0 10
0 5 10 15 20
Storage days (0°C)
Figure 1. Postmortem changes in pH and total volatile base-nitrogen (TVB-N, mg n/100 g of muscle) values in the muscle of
loricariid catfish (Pterygoplichthys disjunctivus) stored in ice (0°C) for 20 days (mean ± SD, n = 5).
JOURNAL OF AQUATIC FOOD PRODUCT TECHNOLOGY 109

storage period. These values fall under the organoleptic acceptability limit (30 mg N/100 g muscle)
for most seafood products (Woyewoda et al., 1986); thus indicating a low spoilage bacteria and
endogenous enzymes activity in the muscle. Chomnawang et al. (2007) showed TVB-N values of
44.37 mg N/100 g muscle at Day 15 on a hybrid catfish stored at 4°C. Similarly, Mohan et al. (2008)
studying catfish (Pangasius sutchi) steaks stored at 0–2°C, reported values of 40.4 mg N/100 g muscle
at Day 20. These studies showed the importance of temperature over TVB-N production in fish
muscle, as the higher the holding temperature for the muscle, the higher the TVB-N values obtained.
A correlation between TVB-N and fish spoilage has been established; however, it depends on species
tested, since levels higher than 30 mg of TVB-N/100 g do not always indicate spoilage, as is the case
of jumbo squid (Dosidicus gigas) (Marquez-Rios et al., 2007), which shows very high values even
minutes postmortem. In this sense, further studies are required to evaluate the correlation between
TVB-N content and sensory properties of loricariid catfish during cold storage.
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

Color analysis
Color is one of the most important parameters used to evaluate quality of seafood products (Haard,
1992). Color parameters in loricariid catfish muscle stored in ice (0°C) did not show any significant
(p < 0.05) change over the first 15 days of the study (Table 1). However, a*, hue angle, and
chromaticity parameters were significantly (p < 0.05) affected upon subsequent storage in ice (0°
C). At Day 20, the parameter a* changed from a brighter red color to a dull grayish-red color,
probably as oxidation of myoglobin occurred. This change obviously affected both the hue angle and
chromaticity of the stored muscle, establishing the muscle color at Day 20 as still in the red-yellow
quadrant but towards dull grayish color, adversely affecting its sensory quality.

Biochemical analysis
ATP postmortem degradation in fish muscle is the result of the endogenous enzymatic activity,
degrading it through the intermediate products ADP, AMP, IMP, HxR, and Hx. The adenosine
nucleotides and their catabolites have been used as freshness indicators in several species. Even
though ATP can rapidly decrease within the first 24 h postmortem (Haard, 1992), adenylated
compound degradation has been a function of fish species and type of muscle (Sikorski et al.,
1990). Results in the present study showed that ATP degradation in loricariid catfish muscle
happened fast, since its content was not higher than 0.6 μmoles/g of muscle at 24 h postmortem
(Figure 2). Adenine nucleotides (ATP, ADP, AMP) rapidly disappeared (p ≥ 0.05) after death, having
values lower than 0.16 μmoles/g at 24 h postmortem. Olafsdottir et al. (1997) reported that in some
species, ATP was rapidly degraded to IMP by endogenous enzymes and further degradation of IMP
to HxR and Hx was much slower. In this study, IMP content was 4.11 ± 1.39 μmoles/g at 24 h
postcatch, decreasing linearly afterwards [IMP μmoles/g = −0.18(d) + 4.07, R2 = 0.95; p < 0.05] to a
final value of 0.45 ± 0.36 μmoles/g at Day 20. Similar results have been reported for Japanese red and
black bream (Ehira and Uchiyama, 1973) and Atlantic haddock and pollock (Dingle and Hines,

Table 1. Postmortem color changes (L* = lightness, +/− a* = redness-greenness, +/− b* = yellowness-blueness, θ = hue angle,
and C = chromaticity) in muscle of loricariid catfish (Pterygoplichthys disjunctivus) stored at 0°C for 20 days.
Storage days L* a* b* Hue angle (θ) Chromaticity(C)
5 44.7 ± 0.8a 8.7 ± 1.5a 6.5 ± 0.5a 37.2 ± 3.2a 10.9 ± 1.4a
8 45.2 ± 0.5a 8.5 ± 1.2a 6.5 ± 0.5a 37.8 ± 2.7a 10.7 ± 1.2a
11 42.7 ± 1.7a 8.3 ± 1.4a 6.5 ± 1.2a 40.4 ± 7.0a 10.6 ± 0.9a
15 43.3 ± 1.4a 6.5 ± 2.3a 6.7 ± 1.5a 46.5 ± 8.9a 9.4 ± 2.3a
20 45.3 ± 2.9a 2.7 ± 1.9b 5.7 ± 1.3a 61.4 ± 13.7b 6.5 ± 1.5b
Data represent the mean and standard deviation of n = 5 for each sampling day. Means in a column with the same letter are not
significantly different (p ≥ 0.05).
110 E. MARQUEZ-RIOS ET AL.

5
ATP
ADP
4 AMP
IMP

micromols/g muscle
HxR
3 Hx

1
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

0
0 5 10 15 20
Storage days (°C)

Figure 2. Postmortem changes in the concentration (μmoles/g of muscle) of ATP and related degradation products in the muscle
of loricariid catfish (Pterygoplichthys disjunctivus) stored in ice (0°C) for 20 days (mean ± SD, n = 5; ATP = adenosine-5´-tripho-
sphate, ADP = adenosine-5´-diphosphate, AMP = adenosine-5´-monophosphate, IMP = inosine-5´-monophosphate, HxR = inosine,
and Hx = hypoxantine).

1971). IMP disappearance has been correlated with a loss of freshness and flavor in some fish species
(Howgate, 2006). This is mainly due to the fact that IMP is responsible for the characteristic sweet,
creamy, meaty flavors of fresh fish muscle (Church, 1998), and also because HxR has no particular
flavor. On the other hand, Hx accumulation, as a result of HxR degradation, gives a bitter taste,
which has also been correlated with loss of freshness and flavor in some fish species and reveals the
initial phase of autolytic deterioration as well as bacterial spoilage (Woyewoda et al., 1986).
Loricariid catfish muscle showed barely detectable initial Hx contents (0.10 μmoles/g) at 24 h
postcapture; however, it increased linearly [Hx μmoles/g = 0.04 (d) + 0.18, R2 = 0.90; p < 0.05] with
time to a final value of 0.99 μmoles/g at Day 20. A slow accumulation of HxR and Hx occurred with
time in this species. Ehira and Uchiyama (1973) defined fish as HxR formers when the ratio of HxR
to Hx was 5:1 and Hx formers when ratio was the inverse. According to this classification, the HxR:
Hx ratio calculated from data at Day 20 of ice storage (1:0.75), indicated that loricariid catfish could
be considered an intermediate HxR and Hx producer species. A similar degradation pattern has been
reported by Greene et al. (1990) for rex sole (Glytocephalus zachirus) and by Li et al. (2011) for
yellow grouper (Epinephelus awoara) in fillets stored under vacuum at 0°C and defined as a typical
characteristic in many fish species (Murata and Sakaguchi, 1986; Ehira and Uchiyama, 1973).
Quantification of ATP concentration and its degradation products until Hx were used as basis to
calculate the K-value or freshness index. Figure 3 shows a significant and linear increase [% K-value
= 3.67(d) + 0.92, R2 = 0.97, p < 0.05] in K-value of loricariid catfish muscle during the storage period,
from 5.61 ± 1.5 % (Day 0) to a final value of 73.17 ± 12.1 % (Day 20). Using this prediction equation,
the K-value at Time 0 was 0.91%. In the literature, fish meat with a Kvalue lower than 20% is
considered as “sushi” or “sashimi” grade or a fish with optimum freshness; fish meat with K-value
higher than 52% but lower than 60% is considered of edible quality; and finally, when the K-value is
higher than 75%, the meat is considered of low quality (Lin and Morrissey, 1994). Rate and change
patterns in adenine nucleotides levels and their related compounds during storage must be calculated
for each type of fish, since patterns differ depending on the fish species, storage conditions, and
muscle types (Murata and Sakaguchi, 1986). Based on these K-value categories and using the
prediction equation, the loricariid catfish muscle would be considered (under the experimental
JOURNAL OF AQUATIC FOOD PRODUCT TECHNOLOGY 111

100

K
80 Ki

% of K and Ki values 60

40

20
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

0
0 5 10 15 20
Storage days (°C)
Figure 3. Postmortem changes in freshness indicators (% of K and Ki) values in the muscle of loricariid catfish (Pterygoplichthys
disjunctivus) stored in ice (0°C) for 20 days (mean ± SD, n = 5).

conditions of this study) very fresh for at least 5 days, moderately fresh up to Day 15, and with a
minimum freshness at Day 20 of ice storage.
Since adenine nucleotides concentration (ATP, ADP, AMP) were very low in the studied species,
a Ki-value was calculated, as a parameter considered to monitor the loss of IMP (Howgate, 2006;
Figure 3). This value was also a good indicator of loricariid catfish freshness with an R2 of 0.965. The
similar behavior of K- and Ki-values indicates that both parameters could be adequate to evaluate
freshness of loricariid catfish muscle.

Microbiological analysis
Microbial activity is responsible for spoilage of most fresh fish products. It is one of the main factors
limiting the shelf life of fresh fish. The initial microbiological quality of loricariid catfish used in the
study was good, as indicated by a low initial number of mesophilic and psychrophilic bacteria (4.2
and 1 log10 CFU g−1, respectively; Table 2). Mesophilic bacteria, which do not easily grow at low
temperatures, practically remained constant when comparing Day 1 to Day 20 of ice storage. All
values remained under the recommended microbiological limits for fish (107 CFU g−1). Similar
mesophilic counts (at Day 1) were found by Mohan et al. (2008), who studied catfish (Pangasius
sutchi) steaks stored at 0–2°C. However, contrary to the present study, the shelf life of their catfish
was seriously affected by this type of microorganism.

Table 2. Microbiological changes in the muscle of loricariid catfish (Pterygoplichtys disjunctivus) stored in ice (0°C) for 20 days.
Storage Mesophilic Psychrophilic Total coliforms Fecal coliforms
days Log10 CFU g−1 Log10 CFU g−1 MPN g−1 MPN g−1
1 4.20 1.00 >1100 < 3.0
3 3.72 1.00 >1100 < 3.0
5 3.17 3.08 290 < 3.0
8 3.39 3.99 240 < 3.0
11 2.63 4.68 240 < 3.0
15 2.95 6.04 3.6 < 3.0
20 4.53 7.70* 93 < 3.0
*Data out of the recommended limits for fresh fish (107 CFU g−1).
112 E. MARQUEZ-RIOS ET AL.

On the other hand, although health regulations do not establish any maximum limit regarding the
psychrophilic counts, they fall under the aerobic microorganisms (total plate count); thus, the
previously mentioned limit, for mesophilic bacteria, can be used to establish fish muscle deteriora-
tion. Besides, this bacterial group can also be responsible for determining the shelf life of any fish
muscle. Microbiologic quality remained under the sanitary standards during this period on ice
storage. In the present study, psychrophilic bacteria counts surpassed the recommended microbio-
logical limits for fresh fish (107 CFU g−1) at more than 15 days of ice storage, indicating that the iced
loricariid catfish muscle would be suitable for human consumption for at least 15 days (assumption
made solely on biochemical and microbiological results). Similar changes in psychrophilic counts
have been reported by Mohan et al. (2008) on catfish (Pangasius sutchi) steaks stored at 0–2°C.
Nevertheless, the loricariid catfish showed a longer shelf life than the Pangasius sutchi (15 versus 10
days, respectively).
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

Some of the parameters used as food sanitary quality indicators are the total and fecal coliforms
presented in the fish muscle. Loricariid catfish showed values higher than 1,100 MPN/g of muscle at
Day 1 of ice storage for total coliforms. Nevertheless, this value was reduced in the subsequent
storage days (down to 3.6 MPN/g), perhaps due to their incapability to adapt at very low tempera-
tures (0°C). On the other hand, fecal coliforms values remained low (< 3 MPN/g of muscle)
throughout the cold storage. In addition, loricariid catfish muscle remained free of pathogens
(Salmonella spp., S. aureus, and Vibrio) throughout the cold storage. These results are an indication
of good hygiene practices while handling the fish and to the absence of these types of microorgan-
isms from the Adolfo Lopez Mateos dam, where the loricariid catfish was captured.

Conclusions
Postmortem changes in loricariid catfish (P. disjunctivus) muscle indicated that both endogenous
and microbial deterioration processes were relatively slow during its storage at 0°C. Physicochemical,
biochemical, and microbiological analyses used proved their usefulness in assessing the quality of
loricariid catfish muscle, while the K- and Ki-values were good indicators in evaluating the fish
freshness during shelf life. Bacterial metabolites that are associated with spoilage and those related to
biochemical endogenous rose at a slow rate during the whole ice storage period, indicating that the
iced loricariid catfish muscle would be suitable for human consumption for 15 days.

Acknowledgments
The authors acknowledge Erika Javier-Saiz for her technical support.

References
Andrews, W. H., Jacobson, A., and Hammack, T. S. 2011. Salmonella. Retrieved from http://www.fda.gov/Food/
FoodScienceResearch/LaboratoryMethods/ucm070149
AOAC. 1993. Official Methods of Analysis of the Association of Official Analytical Chemists (15th ed.). Washington,
DC: Author.
Armbruster, J. W., and Page, L. M. 2006. Rediscription of Pterygoplicthys punctatus and description of a new species of
Pterygolplicthys (Siluriformas: Loricariidae). Neotrop. Ichthyol. 4: 401–409.
Baygar, T., Erkan, N., Mol, S., Özden, Ö., Üçok, D., and Yildirim, Y. 2008. Determination of the shelf-life of trout
(Oncorhynchus mykiss) raw meatball that packed under modified atmosphere. Pak. J. Nut. 7: 412–417.
Bennet, R. W., and Lancette, G. A. 2001. Staphylococcus aureus. Retrieved from http://www.fda.gov/Food/
FoodScienceResearch/LaboratoryMethods/ucm071429
Chomnawang, C., Nantachai, K., Yongsawatdigul, J., Thawornchinsombut, S., & Tungkawachara, S. 2007. Chemical
and biochemical changes of hybrid catfish fillet stored at 4°C and its gel properties. Food Chem. 103: 420–427.
Church, N. 1998. MAP fish and crustacean sensory enhancement. Food Sci. Tech. Today 12: 73–83.
CONANP. 2006. Estudio previo justificativo para el establecimiento de la reserva de la biosfera Zicuirán Infiernillo.
Retrieved from http://www.conanp.gob.mx/anp/consulta/EPJ-Zicuiran.pdf
JOURNAL OF AQUATIC FOOD PRODUCT TECHNOLOGY 113

Dingle, J. N., and Hines, J. A. 1971. Degradation of inosine 5-monophosphate in skeletal muscle of several North
Atlantic fishes. J. Fish. Res. Board Can. 28: 1125–1129.
Ehira, S., and Uchiyama, H. 1973. Formation of inosine and hypoxanthine in fish muscle during ice storage. Bull.
Tokai Reg. Fish. Res. Lab. 73: 63–68.
FAO. 2011. Consumption of fish and fishery products. Retrieved from http://www.fao.org/fishery/statistics/global-
consumption/en
Greene, D. H., Babbitt, J. K., and Reppond, K. D. 1990. Patterns of nucleotide catabolism as freshness indicators in
flatfish from the Gulf of Alaska. J. Food Sci. 55: 1236–1238.
Haard, N. 1992. Technological aspects of extending prime quality of seafood: A review. J. Aquat. Food Prod. T. 1: 9–
27.
Howgate, P. 2006. A review of the kinetics of degradation of inosine monophosphate in some species of fish during
chilled storage. Int. J. Food Sci. Tech. 41: 341–353.
Jiang, S. 2010. Aquaculture, capture fisheries, and wild fish stocks. Resour. Energy Econ. 32: 65–77.
Kaysner, C. A., and DePaola, A. 2004. Vibrio. Retrieved from http://www.fda.gov/Food/FoodScienceResearch/
Downloaded by [University of Sonora], [E. Marquez-Rios] at 08:30 22 January 2016

LaboratoryMethods/ucm070830
Li, X., Li, J., Zhu, J., Wang, Y., Fu, L., and Xuan, W. 2011. Postmortem changes in yellow grouper (Epinephelus
awoara) fillets stored under vacuum packaging at 0°C. Food Chem. 126: 896–901.
Lin, D., and Morrissey, M. T. 1994. Iced storage characteristics of Northern squawfish (Ptychocheilus oregonensis). J.
Aquat. Food Prod. T. 3: 25–43.
Marquez-Rios, E., Moran-Palacio, E. F., Lugo-Sanchez, M. E., Ocano-Higuera, V. M., and Pacheco-Aguilar, R. 2007.
Postmortem biochemical behavior of giant squid (Dosidicus gigas) mantle muscle stored in ice and its relation with
quality parameters. J. Food Sci. 72: 356–362.
Martínez-Palacios, C. A., Campos-Mendoza, A., Díaz-Pardo, E., Arreguín-Sánchez, F., Rueda-Jaso, R., Fonseca-
Madrigal, J., Gutiérrez-Hernández, A., Pacheco-Aguilar, R., Ramirez-Suarez, J. C., Ríos-Durán, M. G., Toledo-
Cuevas, E. M., Salaz-Razo, G., Ross, L. G., Shimada-Miyasaka, A., Viana-Castrillón, M. T., Sánchez-Chinchillas, A.,
Ávila-González, E., and Gasca-Leyva, E. 2010. Bagres Armados: ¿Erradicación o utilización? Cienc. Desarrollo.
36:28–33.
Maturin, L. J., and Peeler, J. T. 2001. Aerobic plate count. Retrieved from http://www.fda.gov/Food/
FoodScienceResearch/LaboratoryMethods/ucm063346.htm
Mendoza, A. R., Escalera, G. C., Contreras, B. S., Koleff, O. P., Ramírez, M. C., Álvarez, T. P., Arroyo, D. M., and Orbe,
M. A. 2009. Directrices trinacionales para la evaluación de riesgos de las especies acuáticas exóticas invasoras: Casos
de prueba para el pez cabeza de serpiente (Channidae) y el pleco (Loricariidae) en aguas continentales de América
del Norte. Retrieved from http://www.biodiversidad.gob.mx/especies/Invasoras/pdf/Directrices_estcaso_espanol.pdf
Mohan, C. O., Ravishankar, C. N., and Srinivasagopal, T. K. 2008. Effect of O2 scavenger on the shelf-life of catfish
(Pangasius sutchi) steaks during chilled storage. J. Sci. Food Agric. 88: 442–448.
Murata, M., and Sakaguchi, M. 1986. Storage of yellowtail (Seriola quinqueradiata) white and dark muscles in ice:
Changes in content of adenine nucleotides and related compounds. J. Food Sci. 55: 321–326.
Ogata, H. Y. 2002. Muscle buffering capacity of yellowtail fed diets supplemented with crystalline histidine. J. Fish Biol.
61: 1504–1512.
Olafsdottir, G., Martinsdottir, E., Oehlenschlager, J., Dalgaard, P., Jensen, B., Undeland, I., Mackie, I. M., Henehan, G.,
Nielsen, J., and Nielsen, H. 1997. Methods to evaluate fish freshness in research and industry. Trends Food Sci.
Tech. 8: 258–264.
Pacheco-Aguilar, R., Ocano-Higuera, V. M., Castillo-Yanez, F. J., Moran-Palacio, E. F., Marquez-Rios, E., and Lugo-
Sanchez, M. E. 2003. Changes in postmortem quality indices in finescale triggerfish muscle stored in ice. J. Food
Biochem. 27: 333–352.
Ryder, J. M. 1985. Determination of adenosine triphosphate and its breakdown products in fish muscle by high
performance liquid chromatography. J. Agric. Food Chem. 33: 678–680.
Sikorski, Z. E., Kolakowska, A., and Burt, J. R. 1990. Postharvest biochemical and microbiologcal changes. In: Seafood:
Resources, Nutritional Composition, and Preservation. Sikorski, Z. E. (Ed.). Boca Raton, FL: CRC Press. Pp. 55–75.
Usydus, Z., Szlinder-Richert, J., Adamczyk, M., and Szatkowska, U. 2011. Marine and farmed fish in the Polish market:
Comparison of the nutritional value. Food Chem. 126: 78–84.
Villalba-Villalba, A. G., Pacheco-Aguilar R., Ramirez-Suarez, J. C., Valenzuela-Soto, E. M., Castillo-Yañez, F. J., and
Marquez-Rios, E. 2011. Partial characterization of alkaline proteases from viscera of vermiculated sailfin catfish
Pterygoplichthys disjunctivus, Weber, 1991. Fish. Sci. 77: 697–705.
Weber, C. 1991. Nouveaux taxa dans Pterygoplichthys sensu lato (Pisces, Siluriformes, Loricariidae). Rev. Suisse Zool.
98: 637–643.
Woyewoda, A. D., Shaw, S. J., Ke, P. J., and Burns, B. G. 1986. Recommended Laboratory Methods for Assessment of
Fish Quality (Canadian Technical Report of Fisheries and Aquatic Sciences No. 1448). Ottawa, ON, Canada:
Fisheries and Oceans Canada. 143 p.

View publication stats

You might also like