DTIC ADA279321: Prevalence of Hepatitis C Viral Antibody in Transfused and Nontransfused Egyptian Children

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P1 BLICATION REPORT
1771
5/94
PREVWALENCE OF HEPATITIS C VIRAL ANTIBODY IN
lt.ANSFUUSED AND NONTRANSPUSED EGYPTIAN CHILDREN
By
M.1 1. E'l-Sayed, N. . llassan, C.1B. kminngs, R.G. Hi~bbs mul A.L. Cowwin
U NAVAL MEDICAL RESEARCH UNIT NO. 3
.S.
(CAIRO, ARAB REPUBLIC OF EGYPI)
PSC 452, BOX 5000
6 'FPO 5 03u'25
S14 AEO09835-O07
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I A',i (14 Y WF ONI Yil' 1i,,) REPORT DATE REPORT TYPE AND DATES COVERED
4. hiLE ANU SUBTITLE 5. FUNDING NUMBERS
Prevalence of Hepatitis C Viral Antibody in Transfused and Non- PE- 62770A
transfused Egyptian Children WU- 3MI62770A870.AR.322
Khalifa, A.S., Mitchell, B.S., Watts, D.M., El-Samahy, M.H.,
El-Sayed, M.H., Hassan, N.F., Jennings, G.B., Hibbs, R.G. and
-Corwin A.L-
1. PI'hltlAMINI ORIAiANILATION NAME(S) AND ADDRESS(ES) 8. PERFORMING ORGANIZATION
REPORT NUMBER
U.S. Naval Medical Research Unit No. 3
PSC 452, Box 5000 5/94
FPO AE 09835-0007
9. SPONSORING /MONITORING AGENCY NAME(S) AND ADDRESS(ES) 10. SPONSORING/ MONITORING
AGENCY REPORT NUMBER
Naval Medical Research and Development
Command, National Naval Medical Center
Building 1, Tower 12
Bethesda, MD 20889-5044
11.SIIi, i'I.EMENTARY NOTES
Published in: Am. J. Trop. Med. Hyg., 49(3):316-321, 1993; Acc. No. 1771.
12a. UISTRIBUTION /AVAILABILITY STATEMENT 12b. DISTRIBUTION CODE
Approved for public release;
Distribution is unlimited.
13. ABSTRACT (Maximum 200 words)
Hepatitis C (HCV) virus is recognized as the major cause of what was previously referred to as parenterally acquired
(blood-mediated) non-A, non-B hepatitis. A study involving 252 transfused and nontransfused Egyptian children was
conducted from November 1990 through February 1991 to determine the prevalence of HCV and the role of blood and
blood and blood product transfusions in the spread of the virus. Serum specimens were assayed by a second generation
enzyme immunoassay and were considered reactive only after supplemental testing using the second generation
recombinant immunoblot assay. Prevalence.among 84 young study subjects with hematologic disorders was 55% (46 of
84), while no HCV antibodies were detected among the two nonhematologic pediatric populations studied: 84 hospital
admissions and 84 acutely ill but otherwise healthy outpatients (seeking treatment for symptoms associated with a new
condition less than three weeks old in the absence of any chronic health problem). Ninety-two percent (77 of 84) of the
hematology-related cases had medical histories of multiple transfusions. Positive antibody responses (46) were
significantly associated with increased duration of illness (P < 0.001) and the volume and number of transfusions (P <
0.01) when compared with negative ones (38). However, prior hospitalization and/or surgery were not related to HCV
antibody status. The high prevalence of HCV antibody among multiply transfused infants and children suggests that
blood and blood product supplies should be regularly screened for HCV antibody.
14. SUBJECT TERMS 15. NUMBER OF PAGES
Hepatitis C virus; Prevalence; Blood transfusions; Blood products; Serology; 6
TrInmfused children; Nontransfused children; Egypt. 16. PRICE CODE
I/. S(cid:127)CIMITirY CLASsIFICATION 10. SECURITY CLASSIFICATION 19. SECURITY CLASSIFICATION 20. LIMITATION OF ABSTRACT
(IF RFI'ORT OF THIS PAGE OF ABSTRACT
UNCLASSIFIED UNCLASSIFIED UNCLASSIFIED
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n.4JL. Trp. Med. H)g.. 49(3)X 1993. pW 316-321
COlghut C 1993 by The Amercan Socict) of Tropi"al Med~ine and HIbew
PREVALENCE OF HEPATITIS C VIRAL ANTIBODY IN
TRANSFUSED AND NONTRANSFUSED EGYPTIAN CHILDREN
A. S. KHALIFA, BENJAMIN S. MITCHELL, DOUGLAS M. WATTS. MONA H.
EL-SAMAHY, MANAL H. EL-SAYED, NASSEF F. HASSAN, GERALD B.
JENNINGS, RICHARD G. HIBBS, AND ANDREW L. CORWIN
Faculty of Medicine..4in Shams University. Cairo.E gVpt; U.S. Naval Medical Research Unit No.
3 (NAMRU-3), Cairo, Egypt; U.S. Naval Medical Research Unit No. 2 (NA4MRU-2), Jakarta,
Indonesia; Naval Environmental Health Center. Norfolk. V'irginia
Abstract. Hepatitis C (HCV) virus is recognized as the major cause of what was pre-
viously referred to as parenterally acquired (blood-mediated) non-A, non-B hepatitis. A
study involving 252 transfused and nontransfused Egyptian children was conducted from
November 1990 through February 1991 to determine the prevalence of HCV and the role
of blood and blood and blood product transfusions in the spread of the virus. Serum
specimens were assayed by a second generation enzyme immunoassay and were considered
reactive only after supplemental testing using the second generation recombinant immu-
noblot assay. Prevalence among 84 young study subjects with hematologic disorders was
55% (46 of 84), while no HCV antibodies were detected among the two nonhematologic
pediatric populations studied: 84 hospital admissions and 84 acutely ill but otherwise
healthy outpatients (seeking treatment for symptoms associated with a new condition less
than three weeks old in the absence of any chronic health problem). Ninety-two percent
(77 of 84) of the hematology-related cases had medical histories of multiple transfusions.
Positive antibody responses (46) were significantly associated with increased duration of
illness (P < 0.00 1) and the volume and number of transfusions (P < 0.0 1) when compared
with negative ones (38). However, prior hospitalization and/or surgery were not related to
HCV antibody status. The high prevalence of HCV antibody among multiply transfused
infants and children suggests that blood and blood product supplies should be regularly
screened for HCV antibody.
Most cases of blood-associated viral hepatitis, Few data are available concerning HCV prey-
including that of community-acquired (sporadic) alence in young children, particularly from North
infections in the absence of non-hepatitis B (HBV) Africa. Findings from healthy adult blood donors
can be attributed to hepatitis C virus (HCV) in- working in Saudi Arabia showed that HCV an-
fections. .2 A particularly high prevalence of HCV tibody prevalence rates among Egyptians (19.2%)
has been found among many European popu- were significantly higher than those of Saudis
lations with chronic liver disease.3 In Taiwan, (1.3%), Sudanese (1.9%), and Yemenis (2.4%).5
HCV infection was found in 43% and 63% of In this report, we present findings on the prey-
hepatitis B surface antigen (HBsAg)-negative pa- alence rates of HCV antibodies in transfused and
tients with cirrhosis and hepatocellular carci- nontransfused Egyptian children.
noma, respectively, although prevalence among
HBsAg-positive patients with chronic liver dis-
ease was significantly lower.' MATERAILS AND METHODS
Hepatitis C virus has been shown to be the
most common cause of post-transfusion hepa- Subjects
titis. Risk groups include dialysis patients and
hemophiliacs. Parenteral transmission has been Two hundred fifty-two children from the Chil-
implicated as the major route in the spread of dren's Hospital of Ain Shams University in Cai-
hepatitis C.1 I In Taiwan, HCV prevalence was ro, Egypt were studied between November 1990
90% among screened hemophiliacs and 8 1% and February 1991 for the presence of antibodies
among parenteral drug abusers, compared with to HCV. Their ages ranged from six months to
1% among voluntary blood donors.' 15 years (mean 6.9 years). Three risk classifica-
316
HCV ANTIBODY PREVALENCE IN EGYPTIAN CHILDREN 317
tions relative to HCV transmission were repre- immunbosorbent assay (ELISA) (Abbott Labo-
sented among the study populations. ratories, North Chicago, IL).
Group I was composed of 84 consecutively Testing of sera for HCV antibodies was carried
selected outpatient cases seen in the Pediatric out at the U.S. Naval Medical Research Unit
Hematology/Oncology Clinic with hematologic No. 3, in Cairo, Egypt. All ELISA testing was
disorders that included beta-thalassemia major initially carried out using a second generation
(24), thalassemia intermedia (three), sickle thai- HCV enzyme immunoassay (Abbott Laborato-
assemia (three), acute leukemias (24), hemo- ries). Patient sera were incubated with polysty-
philia A (10), hemophilia B (two), idiopathic rene beads coated with recombinant (Escherichia
thrombocytopenia purpura (ITP) (eight), hypo- coli or yeast) HCV antigens. At the end of the
plastic anemias (five), autoimmune hemolytic test, samples with absorbance values greater than
anemia (three), and hereditary spherocytosis or equal to the cutoff value were considered ini-
(two). Their mean ± SD age was 7 ± 3.7 years. tially reactive. If positive results were obtained
Group 2 was composed of 84 consecutively upon retesting of the sample, the specimen was
selected hospitalized admissions with nonhe- considered positive for HCV antibodies. Sam-
matoloSic ailments such as rheumatic diseases, pIes that twice showed a positive reaction for
diabetes mellitus, renal disorders, and respira- HCV antibodies were then supplementally tested
tory diseases. Their mean ± SD age was 7.4 ± using a recombinant immunoblot assay (RIBA)
4 years. (Chiron, Emeryville, CA). The antigens C33-C,
Group 3 was composed of 84 consecutively C22-3, 5-1-1, and C100-3 and superoxide dis-
selected children who were seen for acute prob- mutase were present in bands on nitrocellulose
lems that consisted mainly of acute respiratory strips. Following incubation of serum samples
infections and enteric-related conditions at the with the nitrocellulose strips, antigen band in-
hospital's outpatient clinic. Their mean ± SD tensities were compared with weakly positive
age was 6.2 ± 3.7 years. (level I) and moderately positive (level II) IgG
control bands. A response of I + or greater (up
to 4+) to two or more HCV antigens was inter-
Methods preted as a positive result, a response to one
antigen was interpreted as indeterminate, and no
Informed consent was obtained from a parent response to any antigen bands was interpreted as
or legal guardian who accompanied the child to a negative result. Indeterminate results were con-
the hospital prior to inclusion in the study. A sidered negative for the purpose of study anal-
standardized questionnaire was completed for all ysis.
study subjects. This provided an epidemiologic
profile and medical history with an emphasis on RESULTS
the presence or absence of suspected risk factors
associated with HCV transmission. Additional Clinical findings from both histories and clin-
information from children admitted to the hos- ical examinations showed that the hematologic
pital with and without hematologic disorders was subjects (group I) presented with a significantly
obtained from hospital records. Data and spec- more intensive medical profile (percentages) rel-
imen collection procedures were approved by the ative to prior hospitalization and surgery, per-
Naval Medical Research Unit No. 3 Committee sonal and family history of jaundice, and ALT
for the Protection of Human Subjects. values > 30 IU
A thorough clinical examination was con- compared with nonhematologic study popula-
ducted to note the presence or absence of clinical tions (groups 2 and 3). Ninety-six percent (81 of
jaundice, liver span, and the size of the spleen. 84) of study participants in group I had a history
Serum samples were also tested for an elevated of prior blood only transfusions; 95% (77 of 81)
level of alanine transaminase (ALT) (550 Ex- of these had had more than one such transfusion.
press; Ciba-Corning Diagnostics Corp., Med- Also evident was the absence of any history (both
field, MA). A normal ALT level for this assay documented and reported) of blood only trans-
was < 30 IU per liter. Samples were also tested fusions among children in groups 2 and 3. The
for total bilirubin (550 Express; Ciba-Corning mean ALT level was significantly higher among
Diagnositcs Corp.) and an HBsAg enzyme-linked subjects in group I compared with values found
318 KHALIFA AND OTHERS
TAaEi I
Prevalenceo f hepatitis C virus (HCV)a ntibodiesb y group and hematologicc lassification.N ovember 1990 through
Feburary1 9910
Groap I Group 2 Group 3
% (No. postove/ % (No. potiUve/ % (No. postive'
no. tested) no. tested) no. tested)
HCV-2 EIAt 69 (58/84) 1(1/84) 2 (2/84)
RIBAt 79 (46/58) 0(0/!) 0(0/2)
Thalassemiast 73 (22/30)
Acute leukemias* 25 (6/24)
Hemophiliast 83 (10/12)
ITPt 50 (4/8)
Hypoplastic anemiast 60(3/5)
Hereditary spherocytosis* 0(0/2)
Autoimmune anemiat 33 (1/3)
"
For ad efaition ofthe ups ee Subje"ts and MethodL EIA -enzyme immunoay; RIBA - recombinant immunobiot assay ITP - idiopathic
thrombocytopenia purpua.
t Repeat positive (twice positive) using second seneletion EIA.
* Tested by second eenesioe RtBA. all repeat positives (twice positive) were tested by second enetatioa ElA.
in groups 2 and 3 (P < 0.001). Similarly, the among children and infants classified as thalas-
percentage of subjects with an ALT level greater semias (73%) and hemophiliacs (83%).
than 30 IU/I was significantly higher than for the Reactivity to HCV among group 1 study sub-
other two groups (P < 0.001). jects was associated with prolonged duration of
The proportion ofpediatric hematology-relat- illness (Table 2). Children with HCV antibodies
ed cases with HCV antibodies in group I was had a significantly higher mean duration (in years)
55% (46 of 84) (Table 1). No antibody to HCV of illness than those with no detectable antibody
was detected in either groups 2 or 3. In each of (P < 0.001), regardless ofage. The mean volume
the seven hematologic disorders represented in ofblood only transfusions was significantly high-
group 1, except for those with hereditary spher- er among seropositive individuals than among
ocytosis, HCV antibody-positive subjects were seronegative ones (P < 0.0 1). Similarly, the mean
identified. Notable was the high prevalence number of blood only transfusions was greater
among seropositive study subjects, although not
significantly (P > 0.05). Children with evidence
TAnLE 2 of HCV had a significantly higher mean number
Age, sex, and reported and documented medical his- of transfusions when blood products and blood
tories, by hepatitis C virus (HCJ9a ntibody reactivity
(+ or -) determined by en.'yme immunoassay and were factored together (P < 0.001 ).
recombinanti mmunoblot assay, in group I patients, The clinical data in Table 3 show that HCV-
November 1990 through February 1991 positive cases had significantly larger spleens (P
< 0.01) and livers (P < 0.05) than their sero-
Pe,- Pos. negative counterparts. A higher proportion of
tive live
(n -38) (a-46) children with antibodies to HCV also presented
Mean (years) 6 8 with clinical jaundice (P < 0.01). Laboratory
Sex (M:F) 55:45 60:40 findings showed that seropositive subjects had
Mean duration of illness (years) 2 4* higher bilirubin levels (P < 0.05), but there was
History of jaundice (%) 29 37 no evidence that ALT levels were significantly
Family history of jaundice (%) 7 associated with HCV antibody prevalence. How-
History of surgery (%) 18 22
History of hospitalization (%) 79 74 ever, when acute leukemias were excluded from
Mean volume (ml) of transfusions 3,725 4.336t the calculation of mean ALT values, the level in
with blood only children positive for antibodies to HCV was sig-
No. of transfusions with blood only 12 18t nificantly higher than in negative ones (P < 0.05).
(mean units) The presence of HBsAg was detected in both
Nob.l ooofd t rpanrosfduuscitosn s(m weiatnh bulnoiotsd) and 12 27 ppositive and negative HCV cases, with the prev-
b•ood product (meanalence being notably higher among seronegative
f P < 0.01. individuals (P < 0.05).
Y
HCV ANTIBODY PREVALENCE IN EGYPTIAN CHILDREN 319
TABLE 3
Clinik, .features and laboratoryf indings. by hepatitis B virus (HCV) antibody reactivity (+ or -) in group )
patients. November 1990 through February 1991)
HCV neptive HCV poiatiw
(n381 (a-46)
Clinical features
Clinical jaundice (%) 5 22t
Mean liver span (cm) 7(5-1i) 8* (5-15)
Mean spleen size (cm) 2(0-14) 4 (0-15)t
Laboratory results
Bilirubin (direct) (mg/di) 0.07(0.0-0.23) 0.12* (0.0-1.2)
Mean ALT, IU/I 38 (3-155) 34* (5-137)
Mean ALT. WU/I1 20 34*
HBsA&c arrier (N) 19t 7
Vahves is pareamheaatu male. ALT alaime mmntarmita HBsA4 - hqeptitis B surlfce anuam.
tP< 0.01.
IP < 0.0.
Mesa ALT value excluding casa of acute leukemiats.
Table 4 shows a corresponding increase in the respectively (Kostaridou S and others, unpub-
prevalence of HCV antibodies and the increased lished data).
cumulative volume of blood only transfusions. Prolonged duration of illness was significantly
The absolute percent difference (APD) between (P < 0.001) associated with HCV positivity
transfusion levels < 1,200 ml and ? 1,200 ml among patients with hematologic disorders.
but < 4,000 ml (19%) did not differ significantly. Clearly, the number of transfusions required is
However, the percentage of HCV antibody-pos- more likely to increase with the length of illness.
itive cases at the > 4,000 ml level (71%) was Similarly, the mean values pertaining to the vol-
significantly higher (P < 0.01) than at the < ume (blood only) and number (blood only and
1,200 ml level (37%). The risk of infection was blood and blood products) of transfusions were
also linked with the cumulative number ofblood significantly higher (P < 0.01) for seropositive
only transfusions received. The APD between < subjects. These data are further strengthened by
4timesand > 12 times (34%) varied significantly the finding of a parallel between increased prey-
(P < 0.01). alence and increased levels (volume) and num-
bers of blood only transfusions, as shown in Ta-
DISCUSSION ble 4.
Alanine transaminase has been used as a
The prevalence (55%) of HCV antibodies surrogate marker of non-A, non-B hepatitis
found among hematology-related cases, 92% (77 TABLE 4
of 84) of whom had a history of multiple trans- Risk-associated with increased number and volume of
fusions, was higher than seroconversion results blood only transfusions, by hepatitis C virus (HCV)
reported from Swedish and American transfu- antibody reactivity (+ or -) in group I patients, No-
sion recipients.6' This finding is notable in that vember 1990 through February 19910
no antibodies were detected by RIBA among HCV positive
the nonhematologic pediatric controls (n - 168). %( No. poitive/
The prevalence of HCV among Egyptian chil-
_ _ _ __ _ __ _ _
dren with hemophilia (83%) was similar to that Transfusion level (blood only)
reported from Taiwan (90%). Sweden (87%), and < 1,200 ml 37(11/30)
Germany (80%).4. '." High HCV antibody prey- -1,200 ml-<4.000 ml 56(14/25)
alence was also found among other study subjects >4.000 ml 71(20/28)
with hematologic disorders that included thai- No. of transfusions (blood only)
assemias (73%), hypoplastic anemias (60%), and < 4 41(12/29)
MIP (50%). In contrast, prevalence estimates of &4-s1 2 44(10/23)
HCV antibody in patients with thalassemias in >12 75(21/28)
P- 0.0f2or iranifusion leel and 0.019 for no. of transfusions. by
the United States and Greece were 15% and 29%. chi-square test.
320 KJALIFA AND OTHERS
(NANBH)." .7 10 The mean ALT level of HCV- U.S. Naval Medical Research Unit No. 3 (NAMRU-
positive individuals was significantly higher than 3). Cairo, Egypt. Gerald B. Jennings and Andrew L.
Corwin, U.S. Naval Medical Research Unit No. 2
for seronegative individuals only after cases of (NAMRU-2), Jakarta. Indonesia.
acute iekma eeecue rmthe comn-
parison. Thkiasp henen maylubeda riuthed tom Reprint requests: Publications Office, U.S. Naval Med-
parison. This phenomenon may be attributed to ical Research Unit No. 2, Box 3.U nit 8132. APO AP
the chemotherapy nominally administered for 96520-8132.
acute leukemias, namely methotrexate. This
contrasts with other reports that suggest that
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Financial support: This study was supported by U.S. to a hepatitis C virus related protein among pa-
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HCV ANTIBODY PREVALENCE IN EGYPTIAN CHILDREN 321
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forme "
vile Elt
but