AquacultureResearch, 1997, 28, 859865

Use of waste water for aquac ulture: an experimental

eld study at a sewage-treatment plant, Egypt
MT Khalil
Zoology Department, Faculty of Science, Ain-Shams University, Cairo, Egypt
H A Hussein
Microbiology Department, National Centrefor Radiation Research and Technology, Nasr City, Cairo, Egypt
Abstrac t
The primary and secondary treated waste efuents
were successfully used to grow the Nile tilapia
Oreochromis niloticus (L.). The growth rate of sh
reared in treated waste water was signicantly
higher thanthat of shrearedinthenatural habitat.
Bacterial loads in sh organs were higher in the
gills followed by the intestine and the skin and
nallytheediblemuscles. Thetotal aerobicbacterial
count was very low (9.3 10
2
g
1
) in the edible
muscles of sh grown in secondary-treated efuent
and complied with the WHO guidelines (less than
10
5
g
1
). Salmonella, ShigellaandStaphylococcuswere
completely absent in all sh samples examined. The
highest concentrations of heavy metals werefound
in liver tissues, followed by intestine and gills and
then themuscles. Accumulation levels werewithin
the acceptable limits when compared to the
international legal standardsfor hazardouselements
in sh andshery products. In conclusion, chemical
and bacterial analyses indicated that there is no
evidenceof anypublichealthhazardassociatedwith
treatedwastewater reusein aquaculture. However,
therisks, if any, to thesh growers, processors and
consumersshouldbeevaluated, speciallythatrelated
to viral pathogens.
Introduc tion
Fish farminghasvirtually becomethemain hopeof
theEgyptian government for achievingitsoptimistic
animalprotein production targets. However,
because of the shortage of water resources, the
executing authorities have prohibited the use of
freshwater and even drainage water, in some
1997 Blackwell ScienceLtd. 859
regions, for aquaculture. For this reason andin line
with the country policy to control pollution, the
aquaculture authorities directed their efforts for
obtaining new water resources towards recycling
and thereuseof wastewater.
Modern use of treated waste water for sh
production and waste processing demands
examination of its public health implications. In
establishing wastewater-based sh culture, sh
should be sufciently pathogen free and should
contain chemical residues at safe levels.
Zenein Wastewater Treatment Plant, one of six
units, has been constructed through the Greater
Cairo Wastewater Project in 1990. It treats about
330 000 m
3
day
1
, using an oxidation-biological
technique.
The objective of the present study is to evaluate
the reuse of the primary- and secondary-treated
efuent of this plant in aquaculture. Moreover, it
also aims to evaluate the potential public health
threats associated with this practice from both
pathogens and toxic chemicals.
Material and methods
Theprimary treatment of wastewater in this plant
includes screening, grit removal, pre-aeration and
then primary clarication by separatingabout 75%
of thesettleablesolidsfromthewastewater (primary
sludge). In the secondary (nal) treatment, more
than 95%of the solids in the raw waste water is
removed using aerated ponds, activated sludgeand
oxidation ditches. Six ponds were used, each has
thedimensions of 60 mlength, 4 mwidth and6 m
depth. The bottomand banks are made of cement.
Two ponds were fed with primary-treated sewage,
Useof wastewater for aquacultureM T Khalil & H A Hussein AquacultureResearch, 1997, 28, 859865
and two with secondary-treated sewage while the
last two ponds werelled with underground, clean
water for control. For all ponds thewater level was
maintained at a depth of 90 cm.
Twofreshwater sh wereusedin thisexperiment;
theNiletilapia Oreochromis niloticus (Linnaeus) and
the common carp Cyprinus carpio (Linnaeus).
Fingerlings wereobtained fromthehatchery of the
General Authority of Fish Resources Development.
Their average weight was 25.2 g for tilapia and
38.7 g for thecarp.
Both sh were stocked in the ponds at a density
of 100 sh m
3
. The rearing period was 9 months
fromSeptember 1994 to May 1995. The sh were
depending mainly upon plankton as food in the
ponds, but articial supplementary food was
occasionally supplied during therst month.
Waste water samples from the ponds were
subjected, periodically, to physico-chemical analysis
and bacteriological examination according to the
StandardMethods(1992). Thesamplingof sh was
conducted periodically using a small mesh net. The
total length (mm) and weight (g) wererecorded for
each sample sh. Relative growth rates (RGR) of
shes were calculated according to Wrigley, Torien
&Gaigher (1988), as follows:
RGR log
e
(W
f
/W
i
) 100/t
whereRGR is therelativegrowth rateexpressed as
percentagebody massd
1
; W
f
is thenal biomass;
W
i
is the initial biomass and t is the time in days
between W
i
and W
f
.
Also, theaveragedaily gain (ADG) of thesh was
calculated as ADG W
f
W
i
/t.
Microbiological safety of grown sh for human
consumption was examined. Samples fromsh skin
surface, gills, intestine and edible muscles were
assayed for aerobic plate count (APC), coliforms
count, Escherichia coli and Aeromonas hydrophila,
using the surface spread plate technique. The
organisms were detected on nutrient agar,
MacConkey # 3 and starch ampicillin agar
(Palumbo, Maxino, Williams, Buchanan & Thayer
1985). Over agar method was used for isolation of
StaphylococcusaureusandStreptococcusfaecalisusing
Bairparker and Kanamaycin acid media. Isolation
of SalmonellaandShigellawas carriedout according
to ICMSF (1978).
Analysis of theheavy metals, lead(Pb), Zinc (Zn)
and Iron (Fe) in sh edible muscles, gills, liver and
intestine, followed Chernoff (1975). Metal
860 1997 Blackwell ScienceLtd, AquacultureResearch, 28, 859865
concentrations were determined using Pye Unicam
Sp 191 atomic absorption spectrophotometer.
Results and disc ussion
Chemical andmicrobiological characteristics
of treatedwastewater (Table1)
ThepH in thedifferent ponds rangedfrom7.39.8.
These variations were caused by photosynthetic
uptake of CO
2
and bicarbonate; the latter being
substitutedfor hydroxyl ions. Thisexplainsthehigh
pH valuesduringtheday (Ruttner 1963). Dissolved
oxygen (DO) concentrations ranged from 6.8
10 mgl
1
, with an average value of 7.2 and
8.9 mgl
1
in primary and nal efuents,
respectively. Therisein DOconcentration is dueto
the net production of oxygen through
photosynthesis, while the low levels at night are
due to respiratory uptake of oxygen by the pond
biota, especially the phytoplankton. These pH and
DO values are very pertinent for sh aquaculture,
where most of the Egyptian lakes have the same
levels (Khalil 1990).
The raw waste water had a BOD (Biochemical
Oxygen Demand) mean value of 403 mg l
1
. This
value was efciently reduced by 56% (178 mg
l
1
) and 94.3% (23 mg l
1
) through primary and
secondary treatments, respectively. These BOD
removal rates are consistent with that of other
treatment-pond systems (Edwards 1992). The
removal efciencies of COD (Chemical Oxygen
Demand) were40.5%(460 mgl
1
) at theprimary-
treated efuent and 88.4%(90 mgl
1
) at the nal
one. The potential COD removal in other
conventional treatments typically yield a 5872%
reduction (Arthur 1983).
The mean of ammonia nitrogen was 30.3 and
28.3 mgl
1
in primary and nal efuents,
respectively. These levels are considered very high
compared to that of lake waters and even to other
treated waters (El-Gohary, El-Hawary, Badr &
Rashsed 1995).
Lead, zinc and iron were detected during the
analysissurvey for heavy metalsin theprimary and
thenal efuents. Their mean concentration values,
comparedtostandardsset by FAO, werewell within
the established safety range for unrestricted use in
sh culture(WHO1989; Mancy 1993).
Bacteriological examination of primary and nal
treated efuents proved the presence of Escherichia
coli and Staphylococcus aureus, but the complete
AquacultureResearch, 1997, 28, 859865 Useof wastewater for aquacultureM T Khalil & H A Hussein
Table1 Chemical and microbiological characteristics of the raw sewage, treated efuents and underground water of
Zenein plant
Parameter Raw Sewage Primary Efuent Final Efuent Under-Ground Water (Control)
pH 7.3 7.6 7.8 8.4
DO ( mg l
1
) zero 7.2 8.9 10
BO D ( mg l
1
) 403 178 23 19
CO D ( mg l
1
) 772 460 90 21
Suspend solids ( mg l
1
) 387 95 17 12
Alkalinity ( mg l
1
) 290 260 260 350
Ammonia ( mg l
1
) 34.8 30.8 28.3 8.6
NO
3
( mg l
1
) 2.1 7.8 0.9 1.2
PO
4
( mg l
1
) 22.0 26.0 16.8 2
Lead ( mg l
1
) 1.077 1.043 1.042 0.015
Zinc ( mg l
1
) 1.179 1.135 1.129 0.004
I ron ( mg l
1
) 0.790 0.513 0.433 0.034
Total aeorbic count ( No. ml
1
) 2.09 10
7
2.01 10
6
9.0 10
5
4.5 10
4
Coliforms count ( No. ml
1
) 9.1 10
5
5.0 10
3
3.0 10
3

Escherichia coli( No. ml

1
) 1.1 10
4
4.0 10
2
1.0 10
2

Staphylococcus aureus ( No. ml

1
) 1.9 10
3
2.1 10
2
3.3 10
Streptococcus faecalis ( No. ml
1
) 3.7 10
Table2 Fish Performancein treated
wastewater Primary Final Underground
Primary
efuent efuent water
Item
(control)
C yprinus carpio
M ortality ( % ) 100 80 25
O reochrom is niloticus
M ortality ( % ) 39 19 17
Average daily gain/sh ( g) 1.07 1.11 0.917
Specic growth rate 1.33 1.41 1.09
absence of Streptococcus faecalis, Salmonella sp. and
Shigella sp. Most of samples examined for total
aerobic andcoliformscountsin theprimary efuent
did not comply with the WHO (1989) guidelines
(less than 10
5
faecal colifromsml
1
for wastewater
reuse for sh culture), but that of the nal efuent
werevery closeor within theWHOlevels.
The average of phosphate and nitrate levels in
theprimary andnal efuentswasfoundtobevery
high compared to the other water masses in Egypt
(Khalil 1990).
Fish Performancein treated-wastewater
ponds (Table2)
The common carp; Cyprinus carpio faced stress
symptoms, and mortality reached 100% in the
1997 Blackwell ScienceLtd, AquacultureResearch, 28, 859865 861
primary efuent pond after one week and 80%in
the nal efuent after 22 days. All sh examined
showed considerable quantities of mucus on the
skin and gills. The gill lamellae were bleeding.
Vascular congestion occurred in the scaleless skin
on almost the whole body. There were also
haemorrhages in the skin and ns. The caudal n
showed considerable necrosis in the mid
dorsoventral region. Thesesymptomsarecommonly
associatedwithadiseaseknownasInfectiousDropsy
of Carp(IDC) (Seymour 1980). Accordingtoseveral
investigators, this disease is caused by the high
concentration of ammonia levels in the water
(Schaperclaus 1965; Seymour 1980). During the
experimental period, ammonia concentrations
reached to 30.8 and 28.3 mgl
1
in the primary
and nal efuents, respectively. These values were
Useof wastewater for aquacultureM T Khalil & H A Hussein AquacultureResearch, 1997, 28, 859865
considered very high concentrations, compared to
other water masses in Egypt.
El-Gohary et al. (1995) obtained similar results
during their work on a laboratory-scale model to
evaluate the treated efuent for silver carp
aquaculture. Fishesfacedthesamestresssymptoms
and mortality reached 100%after 9 days. During
their study, the ammonia nitrogen range was 0
7.3 mgl
1
; with an averagevalueof 2.7 mgl
1
.
On the other hand, Nile tilapia grew healthy
during the study period in both primary and nal
efuent ponds as well as in theundergroundwater.
The average mortality of tilapia fry in the nal
efuent and underground water (control) was 19
and 17%, respectively, but in the primary efuent
it was as high as 39%. The high percentage of
mortalitymayhaveresultedfromseveral factorsthat
include: (1) signicant differences in the physico-
chemical properties of the water in which the fry
used to live and that of the experimental pond (2)
physiological andmetabolic disorders that occurred
to the fry when subjected to a sudden change into
water that had a high load of bacteria and BOD,
and(3) sensitivity anddistress of thesh under the
various conditions especially during transportation
and after being stocked. Eisawy, Ishak & Hamza
(1974 recorded mortality of thetransplanted fry as
high as 87.5%, due to only transportation distress
and unacclimatization of fry, in their experimental
study torear Mugil cephalus(Linnaeus) in anatural-
water sh farm. The present study suggests that
conditioning and acclimatization of the fry should
becarriedout beforetransportingandstockingthem
in thetreated-efuent rearing ponds may minimize
themortality rate.
The results of this study clearly showed that the
growth rate of the Nile tilapia reared in nal and
primary efuents was higher than that reared in
undergroundwater; beingontheaverage1.11, 1.07
and 0.917 gday
1
per sh, respectively, and the
relative growth rates were 1.41, 1.33 and 1.09,
respectively.
These differences in the growth rates may be
attributed mainly to high levels of nutritive salts;
phosphate and nitrate and sewage, which act as
organic fertilizer, thus increasing the natural
productivity(phytoplankton) of thewater. Morevoer,
this investigation showed that the growth rate of
O. niloticus reared in treated efuent is signicantly
higher thanthatofthenatural habitats. Ishak(1986)
in hisstudy on growth rateof O. niloticusin theNile
water and cage culture indicated that the average
862 1997 Blackwell ScienceLtd, AquacultureResearch, 28, 859865
dailygainwasabout 1.02 gsh
1
. Bayoumi &Khalil
(1988), in their investigation on tilapia sheries of
LakeManzala, recordedaveragedaily gain of about
0.821.08 gsh
1
for O. niloticus. Ontheother hand,
it is noticed that sh reared in treated efuents
maturedmuch earlier (7 months) than thosereared
in undergroundwater (8.5months) andthenewfry
grown in thetreated water ponds werefound to be
healthy. This means that gonads were not affected
histologicallyor physiologicalybythetreated-sewage
water. Bardach, Ryther &Mclarney (1972), Balarin
(1979), Bayoumi &Khalil (1988) and others have
pointedout that tilapiamaturemuchearlier andat a
smaller sizeinresponsetoenvironmental stresses.
Safetylevelsofgrownsh
Bacterial loads(Table3).Generally,thebacterial loads
intilapiaorganswerehighest inthegills, followedby
intestine, skin and nally the muscles. Fish grown
in primary-treatedefuent hadthehighest bacterial
loads. Moreover, coliform bacteria, which are
indicatorsfor thebacteriological qualityofshgrown
inwastewater, appearedonlyinthesesh, although
theywereonlyconnedtogillsandintestineorgans.
It isevident fromtheresultsthat bacterial oraof
theshorgansreect thebacteriological conditionof
water in which they live, especially theskin surface
andgills. But inlivingsh, thebacterial loadsonthe
skinsurfacearekept downandhaveaveryloweffect
due to continuous secretion and sloughing of the
slime.Brown&Dron(1977),Sedik,Safwat,Ibrahim&
Shaaban(1989)andEasa, Shereif, Shaaban&Mancy
(1995) reported also that the ora of the sh was
associated with their environmental conditions and
henceshgrowninpollutedwater maybecarriersof
foodpoisoningtypesof micro-organisms.
Ontheother hand, thetotal aerobicbacterial count
wasverylowinthemusclesofshgrowninsecondary
treated efuent (9.3 10
2
g
1
) as well as
underground water (2.0 10
2
g
1
), while it was
relatively high (8.0 10
4
g
1
) in that of sh grown
intheprimaryefuent, althoughitstill compliedwith
theWHO(1989)guidelines(lessthan10
5
g
1
). These
lowcountsin themusclesamplesmay beduetothe
fact that thereisnodirect contact betweenthemand
water or duetothecapabilityof theimmunesystem
of sh as indicated by Buras, Duek, Niv, Hepher &
Sandbank(1987).
Salmonella sp. and Shigella sp. bacteria were
completely absent in both treated water and sh
AquacultureResearch, 1997, 28, 859865 Useof wastewater for aquacultureM T Khalil & H A Hussein
Table3 Total bacterial and coliforms counts for different organs of sh cultured in treated wastewater (No. g
1
)
Water Source Parameter Gills Intestine Skin Muscles
Primary treated Total bacteria 4.8 10
5
8.5 10
5
3.57 10
5
8.0 10
4
Waste-water Coliforms 6.0 10
2
7.0 10
Secondary treated Total bacteria 2.4 10
5
2.3 10
5
3.2 10
5
9.3 10
2
Waste-water Coliforms
Under-ground water Total bacteria 6.0 10
3
2.0 10
3
1.0 10
3
2.0 10
2
( Control) Coliforms
Table4 Averagesof heavymetal concentrations(gg
1
) inthedifferent organsof O. niloticusgrownintreatedwastewater
during Sept. 1994 to May 1995
Water Source Fish Organ Lead Zinc Iron
Primary treated wastewater Liver 5.02 51.5 7.81
I ntestine 4.41 49.1 6.62
G ills 3.92 45.2 6.10
M uscles 3.01 33.3 4.83
Secondary treated wastewater Liver 4.55 50.8 6.12
I ntestine 2.92 41.4 4.81
nt G ills 2.83 37.7 4.50
M uscles 2.15 30.1 3.51
Underground water ( control) Liver 2.02 24.4 2.92
I ntestine 1.21 18.1 1.93
G ills 1.10 17.2 1.90
M uscles 0.72 13.5 1.30
samples. Thismay bedueto either lowlevelsor the
absenceof themin thetreatedefuents. Sandhya &
Parhand(1988)mentionedthatthestabilizationand
sh ponds are effective systems for Salmonella and
coliformremoval upto99.99%. Slabbert, Morgan &
Wood (1989) isolated Salmonella fromwaste water
but they could not isolateit fromllet sh. Pheleps
(1991) isolatedSalmonellafrom21of90wastewater
samplesandfrom2 of 63 of sh samples. Easa et al.
(1995) attributedtheir failuretoisolateSalmonellato
the effects of the treatment of waste water for the
removal of pathogenic micro-organisms and to the
lowlevelsof theseorganismsintherawwastewater.
StaphylococcusaureusandStreptococcusfaecaliswere
not recovered from the sh samples. This may be
because they are not enteric organisms and they
reach the sh only by contact with dirty boats or
improper handling. This agrees with nding of
Shewan (1971) andEasaet al. (1995) whoreported
that thesebacteria arevery lowor absent on newly
1997 Blackwell ScienceLtd, AquacultureResearch, 28, 859865 863
caught sh but handling, increases their counts
remarkably.
On the other hand, Aeromonas hydrophila was
isolated only from primary and secondary treated
wastewater andalso fromgills of sh grown in the
primary efuent, whilecouldnt beisolatedfromthe
muscles. Gibson, Hendria, Housyton&Hobbs(1977)
found A. hydrophila in fresh water, both clean and
polluted sites, and in salt water. Plumb, Grizzle &
Deftgveriredo (1976) found that A. hydrophila does
not causeanyproblemin thesh population, except
when sh areunder environmental or physiological
stress. Ewing, Hugh &Johnson (1961) recoveredA.
hydrophila from sh, reptiles and water, and they
reportedthat thisorganismisconsideredtobepart of
normal ora of most water systems although
pathogenicity hasbeen demonstratedin both warm
andcoldbloodedanimals.
In conclusion, the microbiological analyses
revealed that there is no evidence of any public
Useof wastewater for aquacultureM T Khalil & H A Hussein AquacultureResearch, 1997, 28, 859865
health hazard associated with wastewater reusein
aquaculture as the edible muscles of sh meet the
bacterial standards recommended by WHO(1989).
Heavymetalslevels(Table4) It isclear fromtheresults
of theexperiment that thehighest concentrationsof
heavy metals were found in liver tissues followed
by intestine, then gills and muscles. This was true
for both primary andsecondary efuent sh, aswell
as, that of the underground water (control). This
meansthat theliver concentratesthesemetalsfrom
the blood circulatory system of the sh. Doi & Ui
(1975), Suffern, Fitzgerald & Szluha (1981) and
Shereif & Moaty (1995) found that heavy metals
were signicantly higher in sh viscera, including
liver tissue, than in theediblemuscletissues.
On the other hand, the results showed that the
heavy metal levelsin thenal efuent sh arelower
than those of the primary efuent ones, but at the
same time, are almost double those found in the
control sh. Generally, it is found that the
accumulation levels of heavy metals of the Nile
tilapia in the present study are within the legal
limits of different countries and WHO guidelines.
For example, in theUnitedKingdomthelegal limits
for lead and zinc in shery products are 2.0
10.0 gg
1
and50 gg
1
, respectively; inAustralia
it is 1.55.5 gg
1
for lead and 40 gg
1
for zinc
(Nauen 1983) while the WHO guidelines are
2.0 gg
1
for lead and 1000 gg
1
for zinc. Saad,
Ezzat, El-Rayis & Hafez (1981) recorded
concentration levels of 7.6 and 11.2 gg
1
for zinc
and iron metals, respectively, in tilapia sh in Lake
Mariut. Moreover, Saad(1987) inhisstudyinNozha
Hydrodrome pond, recorded accumulation levels
of 8.0 and 12.6 gg
1
for zinc and iron metals,
respectively, in tilapia muscles. However, many
investigators(Noble1975; Hejkal, Gerba, Henderson
& Freez 1983; Turner, Sibbald & Hemmens 1986;
Edwards 1992) stated that there may not be a
substantial public health problemproduced by the
bioaccumulation of toxic elements because almost
all organisms contained levels of contaminants
which arebelow Egyptian national legal limits.
In conclusion, thechemical and bacterial studies
revealed that there is no evidence of any public
health hazardassociatedwith wastewater re-usein
aquaculture, especially that subjected to secondary
treatment, asthequality of sh meetsthestandards
recommended by ICMSF (1978) and WHO(1989).
However, more studies are needed to reveal and
864 1997 Blackwell ScienceLtd, AquacultureResearch, 28, 859865
evaluatetherisk of viral pathogensfor sh growers,
processors and consumers.
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