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THE INTERNATIONAL JOURNAL ON NEOTROPICAL BIOLOGY

THE INTERNATIONAL JOURNAL ON GLOBAL BIODIVERSITY AND ENVIRONMENT

Original Article

Percentage Incidences of Bacteria in Mahseer (Tor putitora),

Silver carp (Hypophthalmichthys molitrix) Fish Collected
from Hatcheries and Local Markets of District Malakand and
Peshawar of Khyber Pakhtunkhwa, Pakistan
Incidências percentuais de bactérias em Mahseer (Tor putitora), carpa-prateada
(Hypophthalmichthys molitrix), peixes coletados em incubatórios e mercados locais do
distrito de Malakand e Peshawar de Khyber Pakhtunkhwa, Paquistão.

R. Ullaha* , A. W. Qureshib , A. Sajidc , I. Khanc , A. Ullahc  and R. Tajd 

a
Department of Zoology, Abdul Wali Khan University Mardan, Mardan, Pakistan
b
Department of Zoology, GC Women University Sialkot, Sialkot, Pakistan
College of Veterinary Sciences and Animal Husbandry, Abdul Wali Khan University Mardan, Mardan, Pakistan
c

d
Institute of Chemical Sciences, University of Peshawar, Peshawar, Pakistan

Abstract
Fish is the main source of animal protein for human diet. The aim of this study was to find out prevalence of
pathogenic bacteria of two selected economically important fish of Pakistan namely Mahseer (Tor putitora) and
Silver carp (Hypophthalmichthys molitrix). Live fish samples from hatcheries and dead fish samples from different
markets of study area were randomly collected. The fish samples were analyzed for isolation, identification and
prevalence of bacteria. The isolated bacteria from study fish were identified through biochemical test and about
10 species of pathogenic bacteria were identified including the pathogenic bacteria to human and fish namely,
Pseudomonas aeruginosa, Escherichia coli, Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus iniae,
Serratia spp. Citrobacter spp. Stenotrophomonas spp. Bacillus spp. and Salmonella spp. The bacterial percentage
frequency of occurrence in Silver carp and Mahseer fish showed Pseudomonas aeruginosa 21.42%, Staphylococcus
epidermidis 17.85%, Escherichia coli 11.90%, Staphylococcus aureus 9.52%, Citrobacter spp. 9.52%, Serratia spp. 8.33%,
Streptococcus iniae 7.14%, Stenotrophomonas spp. 5.95%, Bacillus spp. 4.76% and Salmonella spp. 3.57%. The study
revealed that Fish samples of Mahseer and Silver carp that were collected from markets have found more isolates
(10 bacterial species) than did the fresh fish pond samples (03 bacterial species) of hatcheries. The occurrence of
pathogenic bacteria in study fish showed risk factor for public health consumers.
Keywords: prevalence %, bacterial species, Mahseer fish, silver carp fish, biochemical characterization.

Resumo
O peixe é a principal fonte de proteína animal para a alimentação humana. O objetivo deste estudo foi descobrir
a prevalência de bactérias patogênicas de dois peixes economicamente importantes selecionados do Paquistão,
nomeadamente Mahseer (Tor putitora) e carpa prateada (Hypophthalmichthys molitrix). Amostras de peixes
vivos de incubatórios e amostras de peixes mortos de diferentes mercados da área de estudo foram coletadas
aleatoriamente. As amostras de peixes foram analisadas quanto ao isolamento, identificação e prevalência de
bactérias. As bactérias isoladas dos peixes do estudo foram identificadas através de testes bioquímicos e cerca de
10 espécies de bactérias patogênicas foram identificadas incluindo as bactérias patogênicas para humanos e peixes,
nomeadamente, Pseudomonas aeruginosa, Escherichia coli, Staphylococcus aureus, Staphylococcus epidermidis,
Streptococcus iniae, Serratia spp. Citrobacter spp. Stenotrophomonas spp. Bacillus spp. e Salmonella spp. A
porcentagem de freqüência de ocorrência bacteriana em carpa prateada e peixes Mahseer mostrou Pseudomonas
aeruginosa 21,42%, Staphylococcus epidermidis 17,85%, Escherichia coli 11,90%, Staphylococcus aureus 9,52%,
Citrobacter spp. 9,52%, Serratia spp. 8,33%, Streptococcus iniae 7,14%, Stenotrophomonas spp. 5,95%, Bacillus spp.
4,76% e Salmonella spp. 3,57%. O estudo revelou que as amostras de peixes de Mahseer e carpa prateada coletadas
nos mercados encontraram mais isolados (10 espécies bacterianas) do que as amostras de peixes frescos (03
espécies bacterianas) de incubatórios. A ocorrência de bactérias patogênicas nos peixes do estudo apresentou
fator de risco para consumidores de saúde pública.
Palavras-chave: % de prevalência, espécies bacterianas, peixe Mahseer, carpa-prateada, caracterização bioquímica.

*e-mail: [email protected]
Received: May 2, 2021 – Accepted: August 24, 2021
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.

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Ullah, R. et al.

1. Introduction in accordance with the ethics of Society for the Prevention

of Cruelty to Animals (SPCA) of Pakistan.
Fish is the best source of proteins, minerals, vitamins and
essential nutrients that are a supplementary requirement
2.2. Area of study and collection of fish samples.
in diet for infants as well as adults (Abdullah et al., 2011).
Fish contain essential amino acids, low cholesterol and This study was carried out at Mahseer Fish Hatchery
polyunsaturated fatty acids (Adedeji et al., 2011). Among the Thana Malakand and Carp Hatchery and Training center
successfully cultured fish, the Mahseer (Tor putitora) and Peshawar of K.P.K. Pakistan from February, 2018 to
Silver carp (Hypophthalmichthys molitrix) are economically December, 2019. For analysis of prevalence of pathogenic
important fish species in Pakistan (Khan et al., 2011). bacteria two species of fish i.e. the warm water cultural
able Silver carp fish (Hypophthalmichthys molitrix) and
Many methods are used to preserve fish such as cooling
semi cold-water culture able Mahseer fish (Tor putitora)
and freezing (Asiedu and Sanni, 2002). In cold or freezer
were selected. Live fish samples (240) were collected
storage many changes such as biochemical changes in lipids
from both hatcheries and dead fish samples (240) were
and proteins can occur (Latip et al., 2013). The pathogenic
collected from different markets of study area.
bacteria namely, Pseudomonas spp. Salmonella spp. Vibrio
spp. Streptococcus spp. Bacillus spp. Edwardsiella spp.
2.3. Storage and isolation of bacteria from fish samples in
Flavobacterium spp. Corynebacterium spp. Pasteurella spp.
laboratory
Yersinia spp. Shigella spp. E. coli, Proteus spp. Staphylococcus
spp. Serratia spp. Citrobacter spp. Aeromonas spp. Enterobacter After fish collection, immediately samples from skin,
spp. Micrococcus spp. Campylobacter spp. Klebsiella spp. muscles and fins were taken by scraping sterilized cotton
Bacteroides spp. and Hafnia spp. were identified in swab stick after that rubbed cotton swab stick was placed
Tilapia fish (Oreochromis niloticus) tissues collected from in sterile normal saline (0.87% Nacl). Each swab sticks tubes
ponds (Ampofo and Clerk, 2010). Prevalences of bacteria were labeled with name, place and date of collection. The
namely Bacillus cereus, Streptococcus pyogenes, Serratia swab sticks tubes were put on ice packed and transferred
odorifera, Enterobacter amnigenus, Pseudomonas aeruginosa, to laboratory immediately and were stored in refrigerator
Salmonella typhimurium and Shigella flexneri were detected for further bacteriological analysis.
in Rainbow trout (Oncorhynchus mykiss) fish collected
from different trout hatcheries (Kousar et al., 2020). The 2.4. Bacteriological examination through biochemical
bacterial isolates such as Bacillus moratorium, Bacillus characteristics test
pumilus, Bacillus licheniformis, Listeria monocytogenes, Preparation of the media, identification and isolation of
Providential stuartii, Serratia marcescens, Salmonella spp. and bacteria were carried out by applying method described
Staphylococcus saprophyticus were identified in collected by Cheesbrough (1984) and Olutiola et al. (1991).
Tilapia fish (Oreochromis niloticus) from different markets
(Shinkafi and Ukwaja, 2010). When bacteria attached to 2.4.1. Preparation of serial dilutions
any organ of fish at that time are harmless, it becomes In the test tube rack five separates sterilized test tube
harmful after multiplication and production of enzymes (10 ml volume) were arranged serially having 9 ml of
inside fish (Zaman et al., 2011). Whenever the human distilled water for each sample. The contaminated scraped
consumed infected fish with pathogenic bacteria it causes swab sticks were inserted in 1st test tube having 9 ml of
serious diseases such as Vibrio cholerae causes cholera, distilled water and was considered as a stock. The 1 ml
Salmonella spp. causes salmonellosis, Shigella dysentariae, (1000µl) of sample from 1st test tube were picked by
Shigella flexneri, Shigella boydii and Shigella sonnei causes pipette and inserted to second test tube, then it was shake
shigellosis, while Mycobacterium tuberculosis causes TB properly from 2nd test tube up to the 5th test tube were
and Escherichia coli causes dysentery (Okafor, 1985; Austin repeated respectively.
and Austin, 2007).
2.4.2. Inoculation to solid medium
2. Objectives After serial dilution process, 0.1 ml diluted samples
The objectives of our research were to find out were taken and was spread on nutrient agar after that it
prevalence of pathogenic bacteria and its percentage was incubated at 37°C for about 24 hours. Different media
incidences in selected economically important fish namely (MacConkey agar, Mannitol Salt Agar etc) were also used
Mahseer (Tor putitora) and Silver carp (Hypophthalmichthys for specific bacterial isolation.
molitrix).
2.4.3. Gram staining and microscopic examination
From culture plate a colony was picked and then thin
2. Materials and Methods bacterial smear was prepared. Through Crystal violet it
was stained for about one minute then it was rinsed with
water. Few drops of Iodine solution were added for one
2.1. Ethical statement minute then it was rinsed with water. The same smear
This experiment was approved by the ethical review was further washed for 10 to 30 second with decolorized
committee of Abdul Wali Khan University Mardan, agent i-e absolute ethanol after that again rinsed with
Pakistan and further the experimental fish were handled water. Finally Safranin for 30 second to 1 minute was

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 Percentage Incidences of Bacteria in Fish

added and rinsed with water. The slides were dried and 2.4.4.5. Methyl Red / Voges-Proskauer (MR/VP) Test.
were observed with light microscope. For Methyl Red: The suspected colony of bacteria was
incubated for 24 hours at 37°C after that Methyl red reagent
2.4.4. Biochemical characteristics test was added to MRVP broth. For positive result broth turned
After gram staining and microscopic examinations to red color and negative turned to yellow in color.
different biochemical tests were performed for the For Voges-Proskauer (VP): The suspected colony of
identification of bacteria according to the methods as bacteria was incubated in MRVP broth for 24 hours at 37°C
described by Olutiola et al. (1991), Cappuccino and after that few drops of 5% Alpha-naphthol or VP 1 reagent
Sherman (1996), Cowan and Steel (2002), Cheesbrough was added to MRVP broth. The broth was shacked then few
(2006) and Perilla (2003). drops of 40% KOH or VP 2 was added to the same broth.
About 15 minutes waiting in broth red color in ring was
2.4.4.1. Catalase test noticed for positive result.

A drop of 3% H2O2 was added to center of clean slide.

2.4.4.6. Urease test
A colony was mixed with it. The result was interpreted
for positive that is immediate bubbles formation and for In test tubes of urease media, slant were prepared and
negative as no gas formation. colony was inoculated on its surface. After incubation
Control microbes were used for the catalase test: for 24 hours at 37°C the result was interpreted. In the
Staphylococcus spp. = +ve control and Streptococcus positive test result the medium was changed to bright
spp. = -ve control pink color, while in negative test the medium was changed
to yellow color.
2.4.4.2. Oxidase test Control microbes were used for the urease test:
Proteus spp. = Positive control and Escherichia coli =
Oxidase reagent was added to clean filter paper.
Negative control.
A colony was rubbed on it. The result was interpreted for
positive and negative. Positive showed dark blue-purple
color appearance in few second and negative showed no
3. Results
changes in color.
Control microbes were used for the oxidase test:
Pseudomonas aeruginosa = Positive control and 3.1. Identification of bacteria by biochemical test and
Escherichia coli = Negative control prevalence % of the bacterial isolates
The most prevalent isolates bacteria that identified
2.4.4.3. Simmon’s Citrate Utilization Test through biochemical test from study fish were Pseudomonas
In test tubes of citrate media, slant were inoculated aeruginosa, Escherichia coli, Staphylococcus aureus,
with suspected colony. After incubation for 24 hours at Staphylococcus epidermidis, Streptococcus iniae, Serratia
37°C the result was interpreted for positive and negative. spp. Citrobacter spp. Stenotrophomonas spp. Bacillus spp.
Positive showed dark blue color and negative turned to and Salmonella spp. (Table 1). More bacterial isolates i-e
green in color. 10 bacterial spp. were collected from market fish samples
Control microbes were used for Citrate test: of Mahseer and Silver carp, while less bacterial isolates
Klebsiella pneumoniae = Positive control and Escherichia i-e 3 bacteria spp. were collected from fresh samples of
coli. = Negative control Mahseer and Silver carp of hatcheries (Table 2). During this
study, prevalence % of bacterial spp. showed Pseudomonas
2.4.4.4. Sulfur Indole Motility Media (SIM) Test aeruginosa (21.42%), Staphylococcus epidermidis (17.85%),
Escherichia coli (11.90%), Staphylococcus aureus (9.52%),
SIM test tubes were inoculated with suspected colony
Citrobacter spps. (9.52%), Serratia spp. (8.33%), Streptococcus
by straight stabbing. After incubation for 24 hours at 37°
iniae (7.14%), Stenotrophomonas spp, (5.95%), Bacillus spp.
C the result was interpreted.
(4.76%) and Salmonella spp. (3.57%) respectively in collected
For H2S Production: In positive result the media turned
fish samples (Table 3).
to black in color, while in negative no change in color
The study revealed that fresh ponds samples of fish
was observed.
showed good quality as compared to markets fish samples
Control microbe: Proteus mirabilis is positive for H2S
of study area. Pseudomonas aeruginosa showed highest
production.
occurrences (21.42%) followed by Staphylococcus epidermidis
For Motility: The positive result showed movement
(17.85%) and Escherichia coli (11.90%), while Salmonella spp.
from the line of stabbing and negative showed no motility.
showed lowest percentage (3.57%) occurrences (Figure 1).
Control microbes:
Pseudomonas aeruginosa and the strain of Proteus
mirabilis are positive for motility.
4. Discussion
For Indole: Few drops of Kovac´s reagent were added.
In positive result red color ring formation at top of tube In present study the more bacterial isolates in markets
were noticed. fish samples as compared to fresh fish samples was
Control microbe: E. coli is positive for Indole. recorded. The reason behind this might be that in live fish

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Ullah, R. et al.

Table 1. Biochemical test and Microscopy of bacteria species in collected fresh and market fish samples

Gram Methyl Voges SIM

Bacterial Isolates Shape Catalase Oxidase Citrate Urease
staining red proskauer H2S Indole Motility

Pseudomonas - Rod + + - - + - - - +
aeruginosa

Escherichia coli - Rod + - + - - - - + +

Staphylococcus + Cocci + - + + + + - - -
aureus

Staphylococcus + Cocci + - - + - + + - -
epidermidis

Streptococcus iniae + Cocci - - N/A - - - - - -

Serratia spp. _ Rod + - - + + + _ - +

Citrobacter spp. - Rod + - + - + +/- + - +

Stenotrophomonas - Rod + - - - - - - - +
spp.

Bacillus spp. + Rod + +/- - + + N/A - +

Salmonella spp. _ Rod + _ + _ _ _ + _ +

Key: - = Negative reaction, + = Positive reaction, N/A = Not applicable, SIM = Sulfur Indole Motility test, H2S = Hydrogen sulfide.

Table 2. Bacterial isolates in selected fresh and markets fish samples. Table 3. Prevalence % of bacterial isolates in collected fresh and
markets fish samples.
Mahseer Mahseer
and and No. of Prevalence
Bacterial Isolates
Silver Silver Isolates %
Bacterial Isolates
carp carp
Pseudomonas aeruginosa 18 21.42
(Fresh (Market
fish) fish) Escherichia coli 10 11.90

Pseudomonas aeruginosa + + Staphylococcus aureus 08 9.52

Escherichia coli - + Staphylococcus epidermidis 15 17.85

Staphylococcus aureus - + Streptococcus iniae 06 7.14

Staphylococcus epidermidis - + Serratia spp. 07 8.33

Streptococcus iniae - + Citrobacter spp. 08 9.52

Serratia spp. - + Stenotrophomonas spp. 05 5.95

Citrobacter spp. + + Bacillus spp. 04 4.76

Stenotrophomonas spp. - + Salmonella spp. 03 3.57

Bacillus spp. - + Total Isolates 84 100

Salmonella spp. + +
Key: - = Isolates absents + = Isolates presents
indicate that these bacteria came to pond from outside
environments. As described by Jayasinghe and Rajakaruna
their own immunity system can prevent it from bacterial (2005), that many bacteria such as Salmonella, E.coli,
spoilage. As mentioned by Abolagba et al. (2011) that the V. cholera and other coliforms comes from human and
defense system of a fish becomes collapse after the death animal fecal matter to water and become polluted where
of fish which is further attack by microbes. This is further fish survive.
supported by Nwiyi and Onyeabor (2012), that when The result of present study indicated occurrences of
fish is captured, it that time fish can be contaminated by Pseudomonas aeruginosa, Escherichia coli, Staphylococcus
various microorganisms through unhygienic practices aureus, Staphylococcus epidermidis, Streptococcus iniae,
such as use of contaminated equipments, rough handling Serratia spp. Citrobacter spp. Stenotrophomonas spp. Bacillus
and storage facilities. spp. and Salmonella spp. Similarly Shinkafi and Ukwaja
The result obtained in our study indicated that in (2010) reported bacteria in Tilapia fish (Oreochromis
collected fish the pathogenic bacteria i-e Escherichia coli niloticus) that were collected from markets. The finding of
and Salmonella spp. etc were found in pond. The occurrences pathogenic bacteria in this study might leads to zoonotic
of some pathogenic bacteria in fresh samples might infection or intoxication in public health consumers.

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