ISSN 2249-0574 World J Life Sci. and Medical Research 2012;1 1 1 1!! !! !! !!

"a#i$ "a#i$ "a#i$ "a#i$ e% al e% al e% al e% al.& 2012. '(ida%i)e S%ress in *#+hoid ,e)er -a%ien%s

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'ri5inal 'ri5inal 'ri5inal 'ri5inal
6r%icle
Medical
Science
S%a%1s of '(ida%i)e S%ress in *#+hoid ,e)er
-a%ien%s a$on5 ,ishers of 7ala2ar& 7ross
Ri)er S%a%e& Ni5eria
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6cce+%ed36cce+%E Jan1ar#&
2012

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'(ida%i)e S%ress in *#+hoid
,e)er -a%ien%s a$on5 ,ishers
of 7ala2ar& 7ross Ri)er S%a%e&
Ni5eria. World Jo1rnal of Life
Sciences and Medical Research
2012;2!!-G.
Oxidative stress had been known to contribute to some physiological damages in host infected with some
bacteria and viruses. In view of this, the extent of lipid peroxidation and then status of endogenous antioxidants
(ascorbic acid, B- carotene and total cholesterol were (investigated in fishers in !alabar confirmed to be
infected with Salmonella typhi with a view to assessing the status of oxidative stress during the progress of the
disease. "ighty six residents of !alabar, a coastal city in cross river state, were involved in this study. #hey
consisted of $% untreated, $$ on & treatment for % days, $$ confirmed treated patients and $% persons tested to
have no ailment by the time their blood sample were drawn to serve as control. 'esults reveal significant
plasma malondialdehyde (()* elevation (p+,.,- but significant decrease (p+,.,- of the oxidants and total
cholesterol concentrations in patients not yet treated, when compared with those of mean concentrations in
control group. #he results further showed insignificant ()* elevation and antioxidant concentration
diminution in on & treatment and treated groups. #hese results suggest the generation of oxidative stress
during the progress of typhoid fever.
Keywords: Oxidative stress, lipid peroxidation, Salmonella typhii, fishers, !ross 'iver .tate
RHS>MH RHS>MH RHS>MH RHS>MH ? ?? ?,R6NI6IS ,R6NI6IS ,R6NI6IS ,R6NI6IS3,R<N7@A 3,R<N7@A 3,R<N7@A 3,R<N7@A
/e stress oxydatif a 0t0 appel0 1 contribuer 1 certains dommages physiologi2ues dansl3h4te infect0es par des
bact0ries et des virus. )ans cette perspective, la mesure de la peroxydation lipidi2ue et le
statut des antioxydants endog5nes (acide ascorbi2ue, B-carot5ne et de cholest0rol total 0taient (en2u6te che7
les p6cheurs 1 !alabar a confirm0d36tre infect0 par la bact0rie .almonella typhi en vue d30valuer l30tat de le
stress oxydatifau cours de la progression de la maladie. 8uatre-vingt six r0sidents de !alabar, une ville c4ti5re
dans "tat de !ross 'iver, ont 0t0 impli2u0s dans cette 0tude. Ils se composaient de $% non trait0e, $$ sur - le
traitement pendant % 9ours, $$ ont confirm0 les patients trait0s et $% personnes test0es ne pas avoir de mal au
moment o: leur 0chantillon de sang ont 0t0 0tablis pour servir de t0moin. /es r0sultats
r0v5lent significative plasmamalondiald0hyde (()* d30l0vation (p +,,,-, mais diminution significative
(p +,,,- desoxydants et des concentrations de cholest0rol total che7 les patients non
encore trait0s,comparativement 1 celles des concentrations moyennes dans le groupe contr4le. /es
r0sultats ont 0galement montr0 d30l0vation insignifiante ()* et la diminution de
concentration en antioxydant sur - le traitement et les groupes trait0s. !es r0sultats sugg5rent la g0n0ration du
stress oxydatif au cours du d0roulement de la fi5vre typho;de.
Mots-cls: .tress oxydatif, peroxydation lipidi2ue, .almonella typhii, les p6cheurs, "tat de !ross 'iver


IN*R':>7*I'N IN*R':>7*I'N IN*R':>7*I'N IN*R':>7*I'N
Typhoid fever is an infectious disease caused by the
bacterium Salmonella typhii. The disease has several
symptoms in the digestive system in the second phase of
the illness [1, 2]. It is a multisystem illness, characterized
by the classic prolonged fever, sustained bacteremia with
endothelial or endocardial involvement and bacterial
invasion and multiplication within the mononuclear
phagocytic cells of the liver, spleen, lymph nodes and
!ayer patches ["]. It is debilitating and potentially fatal if
untreated. It passes from one person to the other through
contaminated water. Typhoid fever is most prevalent in
many parts of #sia, #frica, $entral and %outh #merica,
where it occasionally causes epidemics [&]. This bacterium
therefore poses problem to fisheries industry since fish
can only be produced in riparian areas
'arlier investigations have revealed that o(idative stress
has been implicated in a number of degenerative diseases
[)]. *ipid peroro(ides, which are free radicals, originate
from the per o(idations of lipids presumably from plasma
World J Life Sci. and Medical Research 2012;1 11 1 !4 !4 !4 !4 ISSN 2249-0574
"a#i$ "a#i$ "a#i$ "a#i$ e% al e% al e% al e% al.& 2012. '(ida%i)e S%ress in *#+hoid ,e)er -a%ien%s



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membrane. !ero(yradicals have been implicated in the
pathogenesis of many disease states such as malaria [+,,],
male infertility [-], sic.le cell anaemia [/], hypertension
[10], tuberculosis [11], trypanosomiasis [12] and many
other disease states [1",1&]. In the present study we
investigated the e(tent of lipid pero(idation inde(ed by
malondialdehyde 123#4 and the status of endogenous
antio(idants 1ascorbic acid, 56 carotene and total
cholesterol4 in volunteers confirmed to be infected with
Salmonella typhi with a view to assessing the status of
o(idative stress during the progress of typhoid fever,

M6*<RI6LS 6N: M<*@':S M6*<RI6LS 6N: M<*@':S M6*<RI6LS 6N: M<*@':S M6*<RI6LS 6N: M<*@':S
In all sub7ects blood samples 1)610 ml4 were collected by
venipuncture into polystyrene tubes and allowed to clot.
%erum was prepared by centrifuging at "000 8 g 19esper
5ench centrifuge4 for 20 minutes the upper layer 1serum4
was collected and used immediately or stored at 20
o
$
until used.

<s%i$a%ion of <s%i$a%ion of <s%i$a%ion of <s%i$a%ion of Li+id -ero(ida%ion Inde( Li+id -ero(ida%ion Inde( Li+id -ero(ida%ion Inde( Li+id -ero(ida%ion Inde(
*ipid pero(idation inde(ed by malondiadehyde 123#4,
was estimated colorimeterically according to the method
of 3as et al. [1)] as adapted by :zoegwu [1+]. # standard
curve was plotted using serial dilutions of the chemical, 1,
1, ", " ; tetraetho(ypropane 1T'!4 which reacts with
hydrochloric acid releasing 23#. The 23# reacts with
thiobarbituric acid 1T5#4 giving a red chromogen. The
chromogen was e(tracted with butan 1;ol and its
absorbance read at )"2 nm using butan; 1; ol as blan..

6ssa# for <ndo5eno1s 6ssa# for <ndo5eno1s 6ssa# for <ndo5eno1s 6ssa# for <ndo5eno1s 6n%io(idan%s 6n%io(idan%s 6n%io(idan%s 6n%io(idan%s
#scorbic acid 1vitamin $4 concentrations were measured
by the method of 9allin et al. [1,]. To 0.) ml of serum, 2.0
ml freshly prepared metaphosphoric acid buffer was
added, mi(ed with a vorle( mi(er and centrifuged for 10
minutes at "000(g. To 1.2 ml of the supernatant, 0.& ml of
dinitrophenylhydrazine6thiourea ; copper sulphate
13T$%4 was added, mi(ed and incubated in a water bath
for " hours. The mi(ture was then chilled for 10 minutes
in an ice bath and 2.0 ml of cold sulphuric acid 112 mol<l4
added slowly. This was again mi(ed with vorte( mi(er,
allowed to stand for "0 minutes at room temperature and
the absorbance read at )20 nm against metaphhosphioric
acid as blan..
; carotene was estimated by the method of Tietz [1-]. To
0.) ml of the test samples 0.) ml of absolute ethanol was
added drop6wise, then sha.en to precipitate proteins.
!etroleum ether 11.0 ml4 was added to each sample, mi(ed
with a vorte( mi(er for ) minutes, and centrifuged for 1
minute at "000 8 g. The separated upper layer was
pipetted out and its absorbance read at &&0 nm against
petroleum ether as blan..

6ssa# for 6ssa# for 6ssa# for 6ssa# for Ser1$ *o%al 7holes%erol Ser1$ *o%al 7holes%erol Ser1$ *o%al 7holes%erol Ser1$ *o%al 7holes%erol
Total cholesterol was determined using commercial assay
.it 1purchased from =ando(, :>4

S%a%is%ical S%a%is%ical S%a%is%ical S%a%is%ical 6nal#sis 6nal#sis 6nal#sis 6nal#sis
?ne way analysis of variance 1#@?A#4 %tatistics for
%ocial %ciences version 1".0 was used to evaluate
significant levels between the different groups of persons.
The results obtained are reported in Bigures 2 ; ) and
Table 1. These show statistically higher significant
increase 1pC0.0)4 in the concentration of 23# in the
untreated and under6 treatment groups compared to the
control. The results also showed a significant decrease
1pC0.0)4 in the concentrations of ascorbic acid, 6$arotene
and total cholesterol in the untreated and under6
treatment groups than in the control group. Burthermore,
the results showed that 23# correlates negatively with
the concentrations of 6carotene 160."-)4 and ascorbic acid
160.12/4 indicating inverse proportional relationship
between them. The correlationship of 23# and total
cholesterol concentration was positive but not significant
1pD0.0)4 10."0,4.

,i51re 1 ,i51re 1 ,i51re 1 ,i51re 1 This figure shows the map of $ross =iver %tate
of @igeria showing study area

ISSN 2249-0574 World J Life Sci. and Medical Research 2012;1 11 1 !5 !5 !5 !5
"a# "a# "a# "a#i$ i$ i$ i$ e% al e% al e% al e% al.& 2012. '(ida%i)e S%ress in *#+hoid ,e)er -a%ien%s



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,i51re 2 ,i51re 2 ,i51re 2 ,i51re 2 This figure shows the mean plasma E6 carotene concentration 1Fg<ml4 of different groups of typhoid fever
patients and the control. 3ifferent letters shows statistically different means



,i51re ! ,i51re ! ,i51re ! ,i51re ! This figure shows the mean plama #scorbic acid concentration 1mg<dl4 of different groups of typhoid fever
patients and control. %ame letters show similar statistical means



,i51re 4 ,i51re 4 ,i51re 4 ,i51re 4 This figure shows the mean plasma cholesterol concentration 1mg<dl4 of different groups of typhoid fever
patients and control. 3ifferent letters mean that the means are statistically different


:IS7>SSI'N :IS7>SSI'N :IS7>SSI'N :IS7>SSI'N
The increased lipid per o(idation as depicted by the high
concentration of 23#, may arise from a variety of factors
such as enhanced generation of free radicals, reduced
level of antio(idants available, enhanced consumption,
lea.age or destruction of antio(idants, decreased
protective capacity including antio(idants enzymes,
lea.age of electrons from the disrupted mitochondrial
electron transport chain and phagocyte recruitment and
activation [1+].
a
c
b
b
b
d
d
c
b
c
a
a
Control Untreated 3 days Treated
on-treatment
Control Untreated 3 days Treated
on-treatment
Control Untreated 3 days Treated
on-treatment
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2embrane lipids succumb easily to deleterious actions of
reactive o(ygen species. The measurement of lipid per
o(idation is a convenient method to monitor o(idative
damage [1/]. In this study the results indicates that serum
concentrations of 23# in the untreated and under6
treatment typhoid patients was significantly higher than
1pC0.0)4 that of the control group. Gigher concentrations
of 23# in severe stages amounts of reactive o(ygen
species were generated as the disease progressed. This
corroborates earlier observation of :zoegwu [1+], who
posits that e(cess reactive o(ygen species could damage
host tissues or cells and the damage to the host cells could
precipitate cell death which is responsible for the
elevation of 23# concentrations in malaria parasite
infected persons. This result is also in consonance with the
observation of the presence of a higher o(idative stress
status in haemodialysis .idney patients when compared
with healthy individuals [20].

,i51re 5 ,i51re 5 ,i51re 5 ,i51re 5 This figure shows the mean plasma 23# 1nmol<ml4 of different groups of typhoid fever patients and control.
3ifferent letters mean that the means are statistically different



*a2le 1 *a2le 1 *a2le 1 *a2le 1 This table shows the correlation between 23# and #scorbic acid, 6 carotene and total cholesterol
7oncen%ra%ion of
M:6 Kn$ol3$lL
7oncen%ra%ion of
ascor2ic acid K$5l3dlL M
$53dlL
7oncen%ra%ion of 2-
caro%ene K$icro53$lL
7oncen%ra%ion of
*o%al choles%erol
K$53$lL
$oncentration of
23# 1nmol<ml4
1 612/ 6"-) 0."0,


#scorbic acid acts as the first line of defence against
o(idative stress during the destructive cycle of typhoid
disease [21]. It is the only antio(idant in serum or plasma
capable of completely inhibiting o(idative modification of
the low density lipoprotein by aHueous pero(yl radical
[21]. 3eficiency of ascorbate also has a direct association
with increased atherosclerosis in guinea pigs and its
inta.e has been shown to have an increased relationship
to atherosclerosis in Huail, rabbit and human [22].
#scorbate administration e(erts a protective role against
pero(idative damage of lipid [22]. %ignificantly lowered
levels of ascorbic acid concentration in the untreated and
under6treatment groups of typhoid patients compared to
the control group may be lin.ed to the increased
consumption of ascorbic acid due to increased reactive
o(ygen species 1=?%4 as evident from enhanced 23#
levels or failure of the system to recycle dehydroascorbic
acid bac. to ascorbic acid. This corroborates the
suggestion that o(idation inactivates and< or depletes
antio(idants and thus in the presence of =?% and
subseHuent lipid pero(idation, antio(idant vitamin
concentration are diminished [/].
6 carotene reacts with lipid pero(idation products to
terminate chain reactions [2"] and also directly scavenge
singlet o(ygen and dissipate the energy as heat [2&]. This
study reveals significant diminution 1!C0.0)4 in the mean
plasma 6 carotene concentrations in the untreated group
of typhoid fever patients when compared with the control
d
b
c
a
Control Untreated 3 days Treated
on-treatment
ISSN 2249-0574 World J Life Sci. and Medical Research 2012;1 11 1 !7 !7 !7 !7
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group while the on6treatment and treated group e(hibited
progressive increase of the 6 carotene could affect the
progress of the disease. This possibility could be
supported by an observation that there was a significant
decrease in the mean serum 6 carotene concentration
with increasing degree of breast cancer [2)]. Burthermore,
low concentration of 6 carotene had been observed to
reflect progression rather than the systemic inflammatory
response in patients with prostate cancer [2+].
?ur study further showed a significant decrease in the
mean serum cholesterol concentration in the untreated
and on6treatment typhoid groups relative to that of the
control groups, perhaps since cholesterol is one of the
preferential targets of o(idation by free radicals. This
observation is consistent with the report of ?labinri, et al.
[2)] who indicated that there was a significant decrease in
the mean total cholesterol in patients with breast cancer
than in the control. %imilarly lower cholesterol level was
reported in tuberculosis patients than in the control due to
=?% attac.s on cholesterol [11].
This study also reveals that 23# concentration correlates
negatively with ascorbic acid and 6 carotene
concentrations as was similarly observed in tuberculosis
patients [11]. It was also observed from the study that
23# correlates positively, though not significantly, with
toya cholesterol indicating that 23# concentration was
directly proportional to this parameter. The insignificant
positive correlation could be as a result of some vagaries
introduced by the assay procedures of total cholesterol.

7'N7L>SI'N 7'N7L>SI'N 7'N7L>SI'N 7'N7L>SI'N
In conclusion, the decreased concentration of endogenous
antio(idants along with elevated malondialdehyde
concentration in typhoid patients could probably be
associated with o(idative stress and< or decreased
antio(idant defense potential. The life threatening
perforation of the patientsI intestinal walls by Salmonella
typhii organism is one of the most outstanding pathologic
involvements of typhoid fever. #lthough, the implication
of o(idative stress in the pathogenesis of typhoid fever is
not investigated in this study, the observed generation of
severe o(idative stress during this disease state could
li.ely indicate that o(idative stress is an essential factor in
the e(acerbation and complications in the pathogenesis of
this disease and therefore, a potential target for therapy. It
could therefore be inferred that increasing the Huantity of
our daily antio(idant inta.e will invariably reduce the
e(tent of lipid per o(idation thereby alleviating the
debilitating effect of o(idative stress generated during
typhoid fever disease.

R<,<R<N7<S R<,<R<N7<S R<,<R<N7<S R<,<R<N7<S
[1] 'astman $. Typhoid Bever and !aratyphoid fever. J.
of Infect. 3is. 1//-),1)4K10)16".
[2] 9ood 2J. 2anagement of Typhoid !atients and its
$omplications. #nn. Int 2ed. 2001+0K1&&6),.
["] $arales =. Typhoid Bever. 200&,
httpK<<www.emedicine com<2'3<topic.2""2.htm
1"1.. #ccessed @ovember 20, 200/.
[&] %chmit %. Typhoid Bever. http<<wwwemedicine.com.
#ccessed @ovember 20, 200/.
[)] 5ayim !5, #da B5, :zuegwu !@. 3iminution in
concentration of free radical scavenger system in
%almonella typhii infections in some fishing
communities of $ross =iver %tate, @igeria. 9orld
Journal of *ife %ciences and 2edical =esearch 2012,
1#ccepted for publication, +<1<20114
[+] Lolenser J, $hevion 2. ?(idant %tress and 2alaria.
Gost !arasite Interrelationship in @ormal and
#bnormal 'rythrocytes. %eminar in Gematology
1//"2+K"1";2).
[,] =ealer =I. ?(idative !rocesses and #ntio(idative
3efense 2echanism in the #ging 5rain. B#%'5
1//),/K)2+6"".
[-] !asHuelotto BB. =elationship between ?(idative
%tress %emen $haracteristics and $linical 3iagnosis
in men under going infertility investigation. Bertile
%terility 2000,"K&)/6+& .
[/] ?gugua A@, 'ze 2?.!lasma *ipid !ero(idation and
#ntio(idant %tatus in %ic.lers, $arriers and @oermal
Individuals. @igerian J. of 5iochem. 2ol. 5iol.
20011+1"4K1)2)6,).
[10] @wan7o G:, ?ze L, ?.afor 2$, @wosu 3, @wan.pa
!. ?(idative %tress and @on6enzymic #ntio(idant
%tatus in Gypertensive !atients in @igeria. #frican J.
of 5iotech. 200,,+11&4K1+-1;&.
[11] @wa.a #$, :zoegwu !@. # $omparism of !lasma
*evels of 2alondialdhyde, Aitamin $ and 56carotene
in 2ale tuberculosis patients and normal individuals.
@igerian J. of 5iochem. 2ol. 5iol. 200) 20114K1/622.
[12] Ihedioha JI, #nwa #!. Burther 'vidence in support of
the #ssertion that ?(idative stress plays a significant
role cellular in7ury in Trypanosome infection.
@igerian J. of 5iochem. 2ol. 5iol. 20011+1"4K&2s6)s.
[1"] $lar. I#. $ell 2ediated Immunity in !rotection and
!athology of 2alaria. !arasitol Today 1/-/"K"006).
World J Life Sci. and Medical Research 2012;1 11 1 !G !G !G !G ISSN 2249-0574
"a#i$ "a#i$ "a#i$ "a#i$ e% al e% al e% al e% al.& 2012. '(ida%i)e S%ress in *#+hoid ,e)er -a%ien%s



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[1&] 2ishra @$, >abilan *, %harma #. ?(idative %tress
and 2alaria ;Infected 'rythrocytes. Ind. J. of 2alaria
1//&"1124K,,6-,.
[1)] 3as 5%, Thurnham 3I, !atnac. J>, 3as 55, #ntipathy
=, 5ase J>. Increase plasma liHuid per o(idation in
riboflavin deficient malaria6infected children.
#merican J. $lin. @utr. 1//0)2K-)/6+".
[1+] :zoeggwu !@. $orrelation of *ipid !ero(idation
Inde( with $oncentration of %ic.le cell Gaemoglobin
of 2alaria !arasite6Infected and :ninfected %ub7ect
of different Gaemoglobingroups in :ga. @igerian
Journal of 5iochemistry and 2olecular 5iology
1%uppl4 20011+1"4K12&6"0.
[1,] 9allin 5, =osengren 5, %hertzer GL, $ame7o L.
*ipoprotein?(idation and measurement of
Thiobarbituric acid reactive substances formation in a
single 2icrotitreplate. #nals of 5iochem. 1//"20-K
106).
[1-] Tietz @@. $arbohydrates in Bundamental of $linical
$hemistry, 95 %aunders $ompany, !hiladelphia,
*ondon 1/,0, p.1,&6+.
[1/] Aiani !. $ervato L, !iorilli, #, $estaro 5. #ge =elated
3ifferences in %ynapatozomal !ero(idative
3amageand 2embrane !roperties. J. of @eurochem
1//1)+K2)"6-.
[20] 9esthuyzen J. 'vidence for ?(idative %tress during
invitro 3ialysis. @ephron 1//) ,0K&/6)&.
[21] Brei 5. #scorbic acid protects liHuids in human
plasma and low density lipoprotein against o(idant
damage. #merican J. clin @utr 1//1)&K 111"s6-s.
[22] %antillo 2, 2ondola !, 2ilone #. #sacorbate
#dimnistrationto normal and $holesterol fed
ratsinhibits invitro T5#=% Bormation in %erum and
liver Gomogenates. *ife %cience 1//+)-K11016-.
[2"] 5urton L9, Lold >:. E6caroteneK an unusual type of
liHuid antio(idant. %cience 1//&22&K),/6-".
[2&] 2athis !, >eleo J. The Triplet %tate 56carotene and of
#nalog !olynes of 3ifferent *engths. !hotochem. and
photobiol. 1/,"1-K"&"6+.
[2)] ?labinri 5@, ?detola ##, #debamowo $#. $hanges
in *evels of %erum E6carotene, Aitamin # and
$holesterol in 5reast $ancer !re6 and !ost6
2enopausal @igerian 9omen. 5iochem 200"1)K226+.
[2+] #lmushatat #%. Aitamins, antio(idants, lipid per
o(idation and systemic inflammatory response in
patients with prostate cancer. Int. J. of cancer
200)1")1-4K20,1s6 "s.

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@o conflict of interests was declared by authors






@o0 %o S12$i% Man1scri+%s
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