RESEARCH Open Access
Dominance o a ian A in Human He pes i us
6 i aemia a e enal ansplan a ion
Esz e Csoma
1*†
, Beá a Mészá os
1†
, Tamás Gáll
1
, László Asz alos
2
, Józse Kónya
1
and Lajos Ge gely
1
Abs ac
Backg ound: Human he pes i us 6 (HHV-6), mos ly a ian B eac i a ion in enal ansplan pa ien s has been
published by o he au ho s, bu he pa hogene ic ole o HHV-6 a ian A has no been cla i ied. Ou aims we e o
examine he p e alence o HHV-6, o de e mine he a ian s, and o in es iga e he in e ac ion be ween HHV-6
i aemia, human cy omegalo i us (HCMV) in ec ion and clinical symp oms.
Me hods: Va ian -speci ic HHV-6 nes ed PCR and quan i a i e eal- ime PCR we e used o examine blood samples
om enal ansplan pa ien s and heal hy blood dono s o he p esence and load o HHV-6 DNA and o
de e mine he a ian s. Ac i e HHV-6 in ec ion was p o ed by RT-PCR, and ac i e HCMV in ec ion was diagnosed
by pp65 an igenaemia es .
Resul s: HHV-6 i aemia was signi ican ly mo e equen in enal ansplan pa ien s compa ed o heal hy blood
dono s (9/200 s. 0/200; p = 0.004), while p e alence o HHV-6 la ency was no signi ican ly di e en (13/200 s.
19/200; p > 0.05). Dominance o a ian A was e ealed in i aemias (8/9), and he equency o HHV-6A was
signi ican ly highe in ac i e in ec ions compa ed wi h la ency in enal ansplan pa ien s (8/9 s. 2/13; p = 0.0015).
La ency was es ablished p edominan ly by HHV-6B bo h in enal ansplan pa ien s and in heal hy blood dono s
(11/13 and 18/19). The e was no s a is ical signi ican di e ence in occu ence o HCMV and HHV-6 i aemia in
enal ansplan pa ien s (7/200 s. 9/200). S a is ical analysis did no e eal in e ac ion be ween HHV-6 i aemia
and clinical symp oms in ou s udy.
Conclusions: Con a y o p e ious publica ions HHV-6A i aemia was ound o be p edominan in enal ansplan
pa ien s. F equency o a ian A was signi ican ly highe in cases o ac i e in ec ion hen in la ency.
Keywo ds: HHV-6, a ian A, enal ansplan a ion
Backg ound
Immunosupp ession associa ed wi h enal ansplan a-
ion p esen s a isk o oppo unis ic in ec ions, eac i a-
ions and ein ec ions. Human he pes i us 6 (HHV-6) is
an impo an pa hogen in ansplan ecipien s. HHV-6
is ubiqui ous in he popula ion, p ima y in ec ion occu s
in ea ly childhood a e which la ency is es ablished and
he se oposi i i y exceeds 90% [1]. The e a e wo dis inc
a ian s o HHV-6 [2]: a ian s A and B (HHV-6A,
HHV-6B). P ima y in ec ion almos always occu s wi h
HHV-6B [3], bu i is no cla i ied when HHV-6A in ec-
ion akes place. HHV-6 in ec ionin ansplan pa ien s
may be he esul o dono ansmission, eac i a ion o
la en in ec ion in he ecipien s o ein ec ion [4]. HHV-
6 eac i a ion occu s ea ly, 38-60% o he pa ien s a e
a ec ed 2-4 weeks a e ansplan a ion [5-7], bu la e
in ec ions up o 2 yea s has been also desc ibed [8,9].
In ec ion is o en asymp oma ic [10], bu eac i a ions
can esul in e e , ash, h ombocy openia, leukopenia,
pneumonia, hepa i is, panc ea i is, coli is, encephali is,
meningoencephali is, e en p olonged bone ma ow
supp ession [4]. HHV-6 can also modula e he immune
sys em which can esul in sp ead and pe sis ence o
HHV-6 and can enhance he e ec s o o he in ec ion
[11]. The e is inc easing e idence o simul aneous eac-
i a ion o HHV-6 and HCMV [12-15], an ac ion which
p edic s highe isk o se e e disease [15]. I is also sug-
ges ed ha HHV-6 eac i a ion occu s ea lie han
* Co espondence: csomae@ eemail.hu
†Con ibu ed equally
1
Ins i u e o Medical Mic obiology, Uni e si y o Deb ecen, Nagye dei k . 98.,
Deb ecen, Hunga y
Full lis o au ho in o ma ion is a ailable a he end o he a icle
Csoma e al.Vi ology Jou nal 2011, 8:403
h p://www. i ologyj.com/con en /8/1/403
© 2011 Csoma e al; licensee BioMed Cen al L d. This is an Open Access a icle dis ibu ed unde he e ms o he C ea i e Commons
A ibu ion License (h p://c ea i ecommons.o g/licenses/by/2.0), which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in
any medium, p o ided he o iginal wo k is p ope ly ci ed.
HCMV [12,14] which may indica e ha HHV-6 can play
a olein he eac i a iono HCMVbyinduc iono
immunosupp ession o by in e ac ion wi h HCMV. In
pe iphe al blood samples o enal ansplan pa ien s
HHV-6 a ian B is mo e equen ly isola ed [16,17], bu
a ian Amaybemo e i ulen [18].Theaimso his
s udy we e o in es iga e he p e alence o HHV-6 in ec-
ion in enal ansplan pa ien s a di e en imes a e
ansplan a ion, o de e mine he sub ype o HHV-6, and
o examine he possible associa ion o HHV-6 in ec ion
wi h HCMV eac i a ion and clinical symp oms.
Resul s
HHV-6 i aemia
Twel e plasma and whi e blood cells (WBC) samples (6%)
o 12 enal ansplan pa ien s we e HHV-6 DNA posi i e.
Dominance o HHV-6 a ian A was e ealed (10/12). The
le el o HHV-6A DNA in plasma samples anged om
7.5 × 10
2
o 6 × 10
5
(median 5.9 × 10
3
)genomeequi a-
len /mL (GEq/mL), while he copy numbe o HHV-6B
genome was below he limi o de ec ion (less hen
250 GEq/mL). In WBC samples HHV-6 DNA load anged
om 5.1 × 10
2
o 2.1 × 10
6
(median 1.8 × 10
3
)GEq/1.5
x10
6
cells. Th ee samples we e nega i e o HHV-6
mRNA, while RT-PCR p o ed ac i e HHV-6 in ec ion in
nine samples (8 HHV-6A and 1 HHV-6B; Table 1).
S a is ical analysis did no e eal signi ican age di e -
ences be ween HHV-6 posi i e ( ange 17.9-61.7 yea s;
median 37.8 yea s) and nega i e (11.2-68.8 yea s; median
45.4 yea s) pa ien s. The e was also no signi ican di -
e ence be ween he ime o sample aking a e he
ansplan a ion o HHV-6 posi i e ( ange 21 days-13.1
yea s; median 6.2 yea s) and nega i e ( ange 3 days-19.6
yea s, median 3.3 yea s) pa ien s.
Among heal hy blood dono s HHV-6 DNA, a ian A
was de ec ed in bo h he plasma and WBC o one sam-
ple; 5.8 × 10
3
GEq/1.5 × 10
6
WBC was measu ed, bu
he i al load in plasma was below he limi o de ec ion.
RT-PCR did no con i m ac i e in ec ion (Table 1).
HHV-6 la ency
HHV-6 la ency was e ealed in 13 enal ansplan
pa ien s (6.5%; 11 HHV-6B and 2 HHV-6A; Table 1).
HHV-6 DNA was de ec ed only in WBC. HHV-6
mRNA was no ound in hese samples.
HHV-6 DNA was ound in WBC wi hou ac i e HHV-
6 eplica ion in 19 heal hy blood dono s (9.5%; 18 HHV-
6B and 1 HHV-6A; Table 1).
HCMV eac i a ion
Se en pa ien s (3.5%) had HCMV eac i a ion shown by
de ec ion o pp65 an igen in WBC.
S a is ical analysis did no show signi ican age di e -
ences be ween HCMV posi i e ( ange 44.1-61.6 yea s;
median 55.4 yea s) and nega i e (11.2-65.7 yea s; median
44.8 yea s) pa ien s. The e was also no signi ican di -
e ence be ween he ime o sample aking a e he
ansplan a ion o HCMV posi i e ( ange 50 days-15.7
yea s; median 0.3 yea s) and nega i e ( ange 21 days-
13.1 yea s, median 6 yea s) pa ien s.
Simul aneous p esence o HCMV and HHV-6 i ae-
mia was no de ec ed.
Clinical da a
Thi y one pa ien s did no ha e clinical symp oms;
e e , espi a o y and gas oin es inal symp oms we e
obse ed in 169 pa ien s (Table 2). All he pa ien s had
good g a unc ions a he ime o he examina ion.
S a is ical analyses o HHV-6 i aemia and clinical
symp oms did no e eal associa ion be ween he p e-
sence o i us and he obse ed clinical symp oms.
Discussion
In his s udy signi ican ly highe p e alence o HHV-6
i aemia was ound among enal ansplan pa ien s hen
among heal hy blood dono s (9/200 s. 0/200; p = 0.004).
The equency o HHV-6 in ec ion was no signi ican ly
di e en om he equency o HCMV eac i a ion
(9/200 s. 7/200; p > 0.05). P e ious epo s ha e no ed
ha HHV-6 i aemia was ound ea ly, bu also la e a e
ansplan a ion [4,13,14]. Signi ican di e ence was no
ound be ween HHV-6 posi i e and nega i e pa ien s
ega ding he days a e ansplan a ion a he ime o
sample collec ion (p > 0.05). HHV-6 is able o es ablish
la ency and in eg a e in o human ch omosomes, hence
i al DNA can o igina e om lysis o cells. The incidence
Table 1 P e alence o HHV-6 and HHV-6 a ian s A and B in enal ansplan pa ien s and heal hy con ols
Vi aemia La ency
T ansplan Heal hy T ansplan Heal hy
HHV-6 (all) 9/200 0/200 13/200 19/200
p = 0.004 p > 0.05
HHV-6B 1/9 0/0 11/13 18/19
HHV-6A 8/9 0/0 2/13 1/19
p = 0.0015
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o ch omosomally in eg a ed HHV-6 (CIHHV-6) is abou
0.2-3% [19-21]. Indi iduals wi h CIHHV-6 ha e signi i-
can i al load, o e million o GEq/mL blood; in ec ion
o eac i a ion usually esul s in only ens o housands
GEq/mL. I is also sugges ed ha inding o a ian A
indica es CIHHV-6 a he hen ac i e in ec ion [20,22].
CIHHV-6 can also be eac i a ed and cells ha bou ing
CIHHV-6 will p oduce in ec ious i al pa icles [23,24].
In his s udy, he i al load de ec ed in he blood samples
o he enal ansplan pa ien s we e in acco dance wi h
a e age DNA load o ac i e HHV-6 in ec ions.
Con a y o some p e ious publica ions [17,25-27],
HHV-6A i aemia was ound o be mo e equen (eigh
ou o nine HHV-6 posi i e samples) in enal ansplan
indi iduals hen HHV-6 a ian B. Nowadays, e ec i e
immunosupp essi e p o ocols wi h new d ugs esul in
imp o ed su i al o g a s in o gan ansplan pa ien s.
Howe e , owing o he s ong immunosupp ession in ec-
ion and consequen ly hospi aliza ion is inc easing among
enal ansplan pa ien s [4]. Nea ly all o he symp oma ic
p ima y HHV-6 in ec ions in child en a e caused by a -
ian B, and HHV-6B is de ec ed p edominan ly in heal hy
indi iduals. HHV-6A has been iden i ied a ely, bu o en
in se e e in lamma o y and neu ological diseases especially
in immunosupp essed pa ien s [28]. HHV-6A dominance
was obse ed in human immunode iciency i us in ec ed
indi iduals,andi may os e he p og ession o AIDS
[11]. HHV-6A may be an eme ging pa hogen, and s ong
immunosupp ession o ansplan pa ien s migh esul in
highe equency o HHV-6A in ec ion. In ou s udy, he
p e alence o la en HHV-6 in ec ion was no signi ican ly
di e en be ween enal ansplan pa ien s and heal hy
blood dono s (13/200 s. 19/200; p > 0.05). Dominance o
a ian B was obse ed in ansplan pa ien s (11/13) and
also in heal hy blood dono s (18/19 la ency). The e-
quency o a ian A was signi ican ly highe in i aemia
hen in la ency in enal ansplan pa ien s (8/9 s. 2/13;
p = 0.0015). HHV-6 a ian A can esul om la ency, p i-
ma y in ec ion o ein ec ion.
S a is ical analysis did no ind in e ac ion be ween
HHV-6 i aemia and clinical symp oms in ou s udy. All
o he pa ien s wi h HHV-6 i aemia had mild diseases a
he ime o sample aking, bu mos o he pa ien s wi h-
ou HHV-6 in ec ion o wi h la ency also had (9/9 s.
160/191; p > 0.05). Ne e heless, i was no a ollow up
s udy, and we ha e no da a be o e and a e he obse ed
HHV-6 i aemia.
HHV-6 and HCMV i aemia was no obse ed simul-
aneously in enal ansplan pa ien s, which does no
exclude he in e ac ion be ween hese i uses.
Conclusions
In his s udy HHV-6 i aemia was de ec ed ea ly and
la e a e enal ansplan a ion. In con as o p e ious
epo s, HHV-6 a ian A i aemia was ound o be p e-
dominan in hese pa ien s. F equency o a ian A was
signi ican ly highe in immunocomp omised pa ien s
wi h ac i e in ec ion hen wi h la ency. A ollow up
s udy o enal ansplan pa ien s may e eal he clinical
impo ance o HHV-6A and i s po en ial pa hogene ical
ole.
Me hods
Pa ien s and samples
Two hund ed EDTA blood samples om 200 enal
ansplan pa ien s (114 men, 86 women, median age
45.5, ange 11.2-68.8 yea s) we e aken a di e en imes
a e ansplan a ion (median 1271 days, ange 3-7115
days). The p e- ansplan HHV-6 se os a us o he
pa ien s was no de e mined. Calcineu in inhibi o , s e -
oid and mycophenola e mo e il was used acco ding o
s anda d immunosupp essi e p o ocols o pa ien s.
Two hund ed EDTA blood samples om 200 heal hy
blood dono s we e also collec ed (75 men, 125 women,
median age 39, ange 10-74 yea s).
Regional and Ins i u ional E hics Commi ee o Uni-
e si y o Deb ecen app o ed all o he s udies. All
pa ien s ga e hei w i en in o med consen .
Table 2 Clinical da a o 200 enal ansplan pa ien s
Numbe o pa ien s
HHV-6+ HHV-6- HCMV+ HCMV-
Respi a o y symp oms 278377
Respi a o y symp oms wi h e e 553157
Respi a o y and gas oin es inal symp oms 1102
Gas oin es inal symp oms 11029
Gas oin es inal symp oms wi h e e 0606
Fe e 012012
No clinical symp oms 031130
To al 9 191 7 193
Csoma e al.Vi ology Jou nal 2011, 8:403
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Page 3 o 5
Quali a i e and quan i a i e PCR o HHV-6
Nucleic acid om whi e blood cells (WBC) (1.5 × 10
6
cells/blood sample) and 200 μL plasma (cen i uged o
10 min a 180 × ga 4°C) was isola ed by High Pu e
Vi al Nucleic Acid Ki (Roche, Swi ze land) acco ding o
he manu ac u e ’s ins uc ions. Nucleic acid was elu ed
in 50 μL and s o ed a -20°C un il usage.
Va ian -speci ic nes ed PCR ampli ica ion o HHV-6
DNA was pe o med in a inal olume o 20 μL con ain-
ing 5 μL DNA solu ions as desc ibed p e iously [29].
To dis inguish be ween la en and ac i e HHV-6 in ec-
ion, e e se ansc ip ion PCR (RT-PCR) was used as
desc ibed p e iously [30].
The e ec i eness o DNA and RNA isola ion we e
con olled by use o PCR and RT-PCR ampli ica ion o
b-globin DNA and GAPDH mRNA.
Absolu e quan i ica ion o HHV-6 DNA using eal-
ime PCR was pe o med ollowing he me hod o Bou-
olleau e al [31]. Fo calib a ion cu e plasmid DNA
(pGL2-Basic ec o , P omega, USA) con aining HHV-6
inse was used.
HCMV pp65 an igenaemia
HCMV eac i a ion was examined by pp65-an igenae-
mia using CINAki (A gene, F ance) acco ding o he
manu ac u e ’s ins uc ions.
S a is ical analysis
Chi sqa e es and Fishe ’s exac es we e used o asses
he di e ence in equency o ca ego ical a iables.
Mann-Whi ney U es was applied o con inuous a i-
ables. Di e ence was conside ed signi ican i p alue
was less hen 0.05.
Acknowledgemen s
This wo k was suppo ed by g an s om he Hunga ian Scien i ic Resea ch
Fund (OTKA 73145).
Au ho de ails
1
Ins i u e o Medical Mic obiology, Uni e si y o Deb ecen, Nagye dei k . 98.,
Deb ecen, Hunga y.
2
Ins i u e o Su ge y, Uni e si y o Deb ecen, Nagye dei
k . 98., Deb ecen, Hunga y.
Au ho s’con ibu ions
ECs con ibu ed o he concep ion and design o he s udy and acquisi ion
o unding, ca ied ou he sample collec ion, nucleic acid isola ion, nes ed
PCR, RT-PCR, i al load assays and d a ed he manusc ip . BM con ibu ed o
he sample collec ion, nucleic acid isola ion, nes ed PCR, RT-PCR. AL
p o ided he clinical samples and clinical da a. TG con ibu ed o posi i e
con ols and plasmid p oduc ion. JK pe o med s a is ical analysis. LG
con ibu ed o he acquisi ion o unding and e ised he manusc ip . All
au ho s ead and app o ed he inal manusc ip .
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Recei ed: 27 May 2011 Accep ed: 15 Augus 2011
Published: 15 Augus 2011
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