Original Article
Evaluation of Antibodies to Hepatitis C Virus in a Study of Transfusion-Associated Hepatitis
N Engl J Med 1990; 323:1107-1112October 18, 1990
- Abstract
- Abstract
Background.
The hepatitis C virus (HCV) is now known to be the chief cause of transfusion-associated non-A, non-B hepatitis, but the prevalence of HCV among blood donors and the frequency of transmission by blood transfusion are unknown.
Methods.
To assess the sensitivity and specificity of a test for antibody to HCV, we tested serum samples from participants in a large study of transfusion-associated hepatitis. Samples were obtained prospectively from consecutive adults undergoing open-heart surgery in Spain, but were tested retrospectively, after the antibody enzyme immunoassay for anti-HCV became available.
Results.
Of 280 transfusion recipients given a total of 1109 units of blood, 27 (9.6 percent) had transfusion-associated non-A, non-B hepatitis (mean follow-up, 52 weeks) and 24 of the 27 seroconverted to anti-HCV—positive, whereas only 2 (0.8 percent) of the remaining transfusion recipients seroconverted. Among the 1044 donor specimens available for testing, 16 (1.5 percent) had anti-HCV antibody. Only 1 additional seropositive donor was found when 44 implicated donors who had been seronegative were retested 9 to 12 months later. Of the 16 recipients of anti-HCV—positive blood, 14 (88 percent) had transfusion-associated hepatitis and seroconverted to anti-HCV—positive. The remaining two recipients had neither hepatitis nor anti-HCV antibody. Among 25 patients with non-A, non-B hepatitis for whom all transfused blood was tested, 14 had received blood positive for anti-HCV.
Conclusions.
About 90 percent of blood donors with antibody to HCV have infectious virus in their blood. The screening of blood donors for anti-HCV antibody should prevent about half the cases of transfusion-associated hepatitis, but the donors with infectious virus who are anti-HCV—negative may remain seronegative for prolonged periods. (N Engl J Med 1990; 323:1107–12.)
Media in This Article
Figure 1
Alanine Aminotransferase and Anti-HCV Profiles in Two Patients with Transfusion-Associated Hepatitis.Table 1
Characteristics of Patients with Non-A, Non-B Transfusion-Associated Hepatitis, According to the Anti-HCV Status of the Donors.*Article Activity
- Article
TRANSFUSION-associated hepatitis has been reported to occur in 2.5 to 15 percent of patients who receive transfusions, and non-A, non-B hepatitis is known to account for the vast majority of these cases.1 2 3 4 5 6 7 8 9 The current incidence of transfusion-associated hepatitis is unknown, since most prospective studies were conducted before 1985, when a number of interventions were instituted by blood banks to prevent human immunodeficiency virus infection. Clinical observation suggests that the exclusion of high-risk donors and the widespread use of surrogate markers in testing may have decreased the incidence of such cases of hepatitis.10 Nonetheless, transfusion-associated non-A, non-B hepatitis remains a serious health problem because of its tendency to become chronic in more than 50 percent of the cases.11 12 13
Researchers have isolated a blood-borne agent of non-A, non-B hepatitis, designated hepatitis C virus (HCV),14 and have developed an immunoassay to detect specific anti-HCV antibodies. The specificity of this immunoassay was established by studying a coded panel of serum samples of proved infectivity in chimpanzees, as well as serum samples from patients with transfusion-associated non-A, non-B hepatitis and from implicated donors.15 The results of these studies clearly showed that the presence of the antibody detected by the assay indicated infectivity rather than immunity to HCV. Subsequent studies indicated that HCV not only is the chief cause of transfusion-associated non-A, non-B hepatitis but also may have a pathogenic role in many cases of chronic liver disease.16 17 18 19 Alter et al.18 reported the presence of an anti-HCV—positive donor in the cases of 14 of 16 patients with transfusion-associated hepatitis C, and seroconversion to anti-HCV positivity occurred in all their patients with chronic transfusion-associated non-A, non-B hepatitis and in 60 percent of those with acute resolving disease.
We report here the investigation of anti-HCV antibody in a group of 280 transfusion recipients recently enrolled in a prospective follow-up study in Spain.
Methods
The Barcelona Post-transfusion Hepatitis Study is an ongoing, multicenter prospective investigation that began in August 1988 as a randomized, double-blind, controlled trial of the efficacy of the use of anti—hepatitis B core antigen and alanine aminotransferase as surrogate markers to decrease the incidence of transfusion-associated non-A, non-B hepatitis. During this early phase of the study all patients undergoing heart surgery who had received transfusions were randomly assigned to receive in a double-blind fashion either blood negative for anti—hepatitis B core antigen and with normal levels of alanine aminotransferase, or blood not screened for these markers. The study was halted in July 1989 with the advent of the anti-HCV test and was converted into an open trial of the efficacy of anti-HCV screening. All patients who had had hepatitis during the study were requested to participate in a randomized, controlled study to evaluate the efficacy of recombinant interferon alfa given during the acute phase. We report here the results of our retrospective evaluation of anti-HCV antibody in the 280 recipients recruited between August 1988 and July 1989, when the randomized study of surrogate markers for HCV was stopped.
Patient Recruitment and Follow-up
Consecutive adult patients undergoing elective open-heart surgery who met our criteria for entry were asked to participate before their anticipated transfusions. Eligibility criteria included an age of at least 18 years; the ability and willingness to provide written informed consent; a prognosis of survival for at least six months; no transfusion within the preceding nine months; no history of viral hepatitis after the age of 12, other than a serologically documented case of hepatitis A; no household, sexual, occupational, or other documented close contact with hepatitis in the preceding six months; no active alcoholism or known liver or biliary tract disease at the time of entry; no exposure to drugs commonly known to increase the level of alanine aminotransferase; and a preoperative level of alanine aminotransferase not more than 1.5 times the upper limit of normal (0.4 μkat [25 IU] per liter).
A 10-ml sample of blood was drawn before surgery, and determinations of alanine aminotransferase, hepatitis B surface antigen, and anti-hepatitis B core antigen were performed. All enrolled patients were randomly assigned to receive either blood negative for anti—hepatitis B core antigen and with normal alanine aminotransferase levels, or unscreened blood. A color code was used to match recipient groups with blood units or components.
Final evaluation for entry into the study was based on the patient's status one week after surgery. The patient's hospital chart was reviewed to determine whether blood had been transfused and in what quantity, and to identify the units by number, the anesthetic agent used, the duration of surgery, and any intraoperative or postoperative complications. Patients who had not received transfusions or who had received commercial clotting-factor concentrates were excluded at this time.
For eligible patients, four additional visits were scheduled 6, 8, 12, and 24 weeks after transfusion. In addition, the patients were requested to contact one of the investigators if any clinical symptoms appeared before or between scheduled visits. At each visit the patient's status was reviewed and a blood sample obtained. For patients living outside Catalonia, blood specimens were drawn at local laboratories, which measured alanine aminotransferase and sent the specimens to the study center within 24 hours. Follow-up was discontinued if there was a further transfusion or any recognized exposure to viral hepatitis.
After the first clinical or biochemical evidence of viral hepatitis, visits and blood sampling occurred weekly or biweekly for six months and monthly thereafter.
Definition of Events
A diagnosis of hepatitis was made if between 4 and 24 weeks after transfusion the serum level of alanine aminotransferase exceeded 2.5 times the upper limit of normal (i.e., 1 μkat [62.5 IU] per liter) and a repeat value 1 to 2 weeks later exceeded 2 times the upper limit of normal (i.e., 0.8 μkat [50 IU] per liter), and other possible explanations for the elevation (the use of hepatotoxic drugs or severe right-sided heart failure, for example) had been excluded. The diagnosis of non-A, non-B hepatitis was established after infection with hepatitis A, hepatitis B, cytomegalovirus, and Epstein–Barr virus had been excluded by standard serologic criteria. Progression to chronic disease was established if alanine aminotransferase values were still elevated more than six months after the acute phase, if a liver biopsy showed unequivocal signs of chronic hepatitis, or both.
Laboratory Procedures
Alanine aminotransferase was measured in donors and recipients within six hours after the samples had been obtained, with use of a kinetic assay with commercial reagents (Boehringer–Mannheim, Mannheim, Germany) at 25°C in an AutoAnalyzer (Hitachi, Tokyo). The level of alanine aminotransferase in donor samples was considered elevated if it exceeded 0.5 μkat (30 IU) per liter. Tests for anti—hepatitis B core antigen were also performed in donor samples within six hours after donation, with use of a commercial enzyme-linked immunosorbent assay (ELISA; Behringwerke, Marburg, Germany). Tests for hepatitis B surface antigen, IgM anti—hepatitis B core antigen, IgM anti—hepatitis A virus, anti—cytomegalovirus, and anti—Epstein–Barr virus antibodies were performed with commercial kits (Abbott Diagnostic Systems, Abbott Park, Ill.).
Half the recipients were given blood that was negative for anti—hepatitis B core antigen and had normal levels of alanine aminotransferase, and the other half received blood that had not had this additional screening. All serum samples from donors and transfusion recipients were stored at −30 to −70°C. These samples were later tested for anti-HCV antibody with the antibody ELISA recently developed by Chiron Corporation (Emeryville, Calif.) and Ortho Diagnostic Systems (Raritan, N.J.). In the new assay a recombinant polypeptide antigen (C-100–3) attached to the wells of a microtiter plate captures specific antibodies present in the serum, and these are then identified by a secondary enzyme-labeled monoclonal anti—human IgG antibody and the appropriate substrate. Once the reaction is complete, the optical density of each well is measured at 492 nm. Positive reactions must have readings above the mean optical density of three negative control wells and a constant (0.400). All initially reactive samples were retested in duplicate. The ELISA ratio of each reactive sample was expressed as the mean ELISA ratio (the optical density of the sample divided by the cutoff value) of the three tests. All donor samples repeatedly reactive on ELISA were tested with use of the Chiron recombinant immunoblot assay (RIBA)—HCV test system. RIBA testing was performed as indicated by the manufacturer. Briefly, a 1:50 dilution of the sample was incubated with a nitrocellulose strip precoated with the recombinant peptides produced by HCV-specific clones 5.1.1 and C-100.14 , 15 After washing, the strip was incubated with a secondary enzyme-labeled goat anti—human IgG antibody. The presence of bound antibody was identified with an appropriate substrate. A sample was considered reactive if the two bands corresponding to the 5.1.1 and C-100 peptides were simultaneously present.
The titer of anti-HCV antibody in reactive samples was defined as the end-point dilution obtained by testing (at the working dilution of 1:10 recommended by the manufacturer) serial twofold dilutions of the sample in a normal human serum pool unreactive for anti-HCV.
Statistical Analysis
The results are given as means ±SE. A chi-square or Fisher's exact test was used to determine the two-tailed statistical significance of differences between proportions in two-by-two tables, and Student's t-test was used to evaluate the significance of differences between normally distributed continuous variables. For variables that were counts with highly skewed distributions, the Mann—Whitney U test and Spearman's rank-correlation test were used. An alpha of 0.05 was used as the indicator of statistical significance. All P values were two sided. A multiple logistic-regression model with maximum-likelihood estimation of parameter values was used to determine the independent contributions of the number of units received and the serologic status of the donors (anti-HCV—positive, elevated alanine aminotransferase level, or both) in predicting the occurrence of transfusion-associated hepatitis. Adjusted odds ratios and 95 percent confidence intervals were derived from logistic-regression coefficients to provide an estimate of the statistical association between a given variable and the occurrence of hepatitis, with the other variables held constant.
Results
Of the 350 transfusion recipients initially enrolled in the study, 70 (20 percent) were later excluded from analysis: 18 (5 percent) were found to be ineligible during the immediate postoperative evaluation (elevated levels of alanine aminotransferase before surgery in 5, recent blood transfusion or the administration of clotting-factor concentrate during surgery in 5, active alcoholism in 4, and severe right-sided heart failure in 4); 34 (10 percent) died within 10 weeks after surgery; and 18 (5 percent) were lost to follow-up. This analysis thus involves the remaining 280 recipients, who received a total of 1109 units of blood (3.9±0.23 units per patient) and who have been followed for a mean of 52 weeks (range, 31 to 75).
Cases of Hepatitis
Overall, non-A, non-B hepatitis developed 4 to 11 weeks (mean, 6.9±0.27) after transfusion in 27 patients (9.6 percent) who had received a mean of 5.9±0.9 units of blood and who were followed for a mean of 54 weeks (range, 34 to 74). No statistically significant differences were found in the incidence of hepatitis between the recipients of unscreened blood and the recipients of blood screened for anti—hepatitis B core antigen and alanine aminotransferase level (data not shown). Only 7 of the 27 patients (26 percent) had jaundice. Seven patients were randomly assigned to receive a three-month course of interferon therapy.
Anti-HCV Testing
Of the 1044 donor samples (from 94 percent of all donors) available for testing, 16 (1.5 percent) were found to be repeatedly reactive for anti-HCV antibody; 2 had ELISA ratios between 1 and 2, 4 had ratios between 2 and 5, and the remaining 10 had ratios above 5. On RIBA, all samples were reactive for both the 5.1.1 and C-100 polypeptides, irrespective of their ELISA ratio, titer, and the outcome in the corresponding recipient. The mean antibody titer, as estimated by testing serial twofold dilutions of each reactive sample, was 1:16 (range, 1:2 to 1:256). Components from the 16 seropositive units had been transfused to 16 different recipients, 14 of whom (88 percent) had non-A, non-B hepatitis and seroconverted to anti-HCV—positive; the remaining 2 recipients of a seropositive unit did not acquire hepatitis, nor did they seroconvert to anti-HCV—positive during more than nine months of follow-up. In contrast, of the 217 recipients of blood negative for anti-HCV antibody, only 11 (5 percent) acquired non-A, non-B hepatitis. (There were 233 sets of serum samples available for testing; 47 sets were incomplete and were excluded from analysis.) Hence, the estimated relative risk of hepatitis associated with blood positive for anti-HCV antibody was 137 (95 percent confidence interval, 28 to 681).
As of March 1990, 8 to 35 weeks after transfusion (mean, 15±1.3), 24 of the 27 patients with non-A, non-B hepatitis had seroconverted to anti-HCV—positive (89 percent). The remaining three patients, who were followed from 39 to 58 weeks, all received a three-month course of interferon therapy during the acute phase of the disease. On the other hand, there were significant variations in the antibody profile among those who seroconverted (Fig. 1Figure 1
Alanine Aminotransferase and Anti-HCV Profiles in Two Patients with Transfusion-Associated Hepatitis.). Seroconversion was transient in two patients, whose low-titer anti-HCV antibody lasted for 6 and 10 weeks, respectively; in both cases the disappearance of the antibody was confirmed during subsequent follow-up (for 36 weeks in one and 46 in the other) and was accompanied by persistently normal levels of alanine aminotransferase. In the remaining patients anti-HCV antibody persisted throughout subsequent follow-up. In general, the antibody profile correlated poorly with the levels of alanine aminotransferase; although in some cases normalized alanine aminotransferase values seemed to be accompanied by a decrease in antibody titer, in others the titer increased when the alanine aminotransferase values returned to normal.To investigate whether the 11 recipients of seronegative blood might have received a unit from an infected donor who was in a window period (the interval from HCV infection to anti-HCV seroconversion) at the time of donation, 44 of their 49 donors were retested 9 to 12 months after the implicated donation; only 1 donor was found to be repeatedly reactive for anti-HCV antibody in the sample obtained 50 weeks after the donation. Of the eight recipients whose complete sets of donors were retested, only one seemed to have been infected by a donor who had not seroconverted at the time of donation.
As shown in Table 1Table 1
Characteristics of Patients with Non-A, Non-B Transfusion-Associated Hepatitis, According to the Anti-HCV Status of the Donors.*, when the 25 patients with complete data on the donors were subdivided according to whether they had received a unit positive for anti-HCV antibody, no significant differences were found with respect to incubation period, presence of jaundice, peak alanine aminotransferase level, time to seroconversion, mean anti-HCV titer, and outcome. Of these 25 patients with transfusion-associated hepatitis, 14 (56 percent) had received anti-HCV—positive blood. (The other two patients with transfusion-associated hepatitis were excluded from the analysis of risk because not all donor samples were available for testing.)When samples obtained six months after transfusion from the 280 recipients were tested for anti-HCV antibody, 37 (13 percent) were positive. Twenty-four were from the recipients with hepatitis who had seroconverted. In 11 additional patients, the corresponding preoperative sample was also found to be positive, and they were thus considered to have had a previous exposure unrelated to the recent transfusion (only 2 patients had received earlier transfusions); in all 11 the alanine aminotransferase values had remained within normal limits during follow-up. Finally, the remaining two patients whose preoperative sample was negative for anti-HCV antibody were found to have seroconverted after the transfusion of one and seven units of seronegative blood, respectively; in both patients the alanine aminotransferase levels were elevated but did not reach the values required for a diagnosis of transfusion-associated hepatitis in some of the follow-up samples.
Variables that might be associated with a greater risk of transfusion-associated hepatitis were analyzed, as shown in Table 2Table 2
Incidence of Non-A, Non-B Hepatitis among Transfusion Recipients, According to Demographic Characteristics, Number of Units Transfused, History of Transfusion, and Serologic Status of the Donors.. Although age, sex, and history of blood transfusion did not influence the incidence of hepatitis, recipients of more than five units of blood had a significantly higher incidence of transfusion-associated hepatitis than those who had received five or fewer units (20 vs. 7 percent, P = 0.001). The recipients of a unit positive for anti-HCV antibody had a significantly higher incidence of hepatitis than those who received only seronegative blood (88 vs. 5 percent, P<0.001). Similarly, the recipients of blood with alanine aminotransferase levels ≥0.5 μkat (30 IU) per liter had a higher incidence of hepatitis than those who received blood with normal levels (33 vs. 7 percent, P = 0.033).When these three variables were analyzed in a logistic-regression model to determine their relative importance as predictors of hepatitis in the recipient, a donor positive for anti-HCV antibody was found to be the only independent variable associated with a higher risk of hepatitis in the recipient (odds ratio, 193; 95 percent confidence interval, 29 to 1265; P<0.001).
Discussion
The objective of the present study was to provide practical information about the performance of the anti-HCV test in unselected serum samples from pairs of donors and recipients participating in a prospective follow-up study of transfusion-associated hepatitis.
The finding that all but 3 of the 27 patients in whom hepatitis developed seroconverted to anti-HCV—positive confirms the previously reported observation that the vast majority of cases of transfusion-associated non-A, non-B hepatitis are caused by HCV.16 17 18 19 Whether the lack of seroconversion in three recipients of blood negative for anti-HCV antibody was related to the interferon therapy they received during the acute phase of the infection remains speculative. The occurrence of seroconversion in three other similarly treated patients would argue against such a relation. On the other hand, the possibility that those who did not seroconvert represented cases of transfusion-associated hepatitis due to another agent of non-A, non-B hepatitis cannot be excluded.
In the present study, only 56 percent of the patients with transfusion-associated hepatitis had received a unit of blood positive for anti-HCV antibody. Since we have recently observed that 36 percent of anti-HCV—positive donors in our area have elevated alanine aminotransferase levels and 18 percent are positive for anti—hepatitis B core antigen antibody (unpublished data), it is possible that this rather low figure may be explained in part by the fact that half the recipients in the study received blood that had been screened for these surrogate markers.
Since it has been observed that in some patients with transfusion-associated HCV, seroconversion to anti-HCV—positive may be delayed for one year, Alter et al.18 have suggested that the transmission of HCV by seronegative blood may be expected to occur if people infected with the virus donate blood during the window period. In the present study, however, only 1 of 44 initially seronegative implicated donors was found to be weakly but repeatedly reactive on retesting almost one year later. Therefore, although donation during the window period may explain HCV infection in some recipients of blood negative for anti-HCV antibody, this mechanism does not explain the majority of cases of HCV transmission by seronegative blood in our study. Instead, our findings indicate that a carrier state of infectious HCV may be common in the absence of detectable levels of antibodies to the HCV-specific recombinant C-100–3 polypeptide on which the current assays are based. This observation has important implications, not only concerning the efficacy of anti-HCV screening in reducing transfusion-associated hepatitis, but also in the interpretation of seroconversion after acute HCV infection. Consequently, in view of our findings, it is not possible to predict whether or to what extent the normalization of alanine aminotransferase values and clearance of anti-HCV antibody imply complete recovery from infection. To address this issue, extensive evaluation of such cases by means of sensitive techniques to detect HCV RNA in blood and tissue will be required.
Three findings of this study were unexpected and deserve further comment. First, HCV infection occurred in two recipients of seronegative blood in the presence of a moderate and fluctuating increase in alanine aminotransferase levels that did not reach the values required for a diagnosis of hepatitis despite unequivocal seroconversion to anti-HCV-positive. This might indicate either that a high level of HCV replication (accompanied by high levels of alanine aminotransferase, reflecting the destruction of liver cells by this cytopathic virus) is not always needed to elicit a detectable antibody response, or that there are HCV variants that replicate at levels sufficient to elicit an antibody response despite inducing minimal liver-cell necrosis. In contrast, in two instances the transfusion of seropositive units apparently did not result in HCV infection in the recipients. Whether seropositive donors do not have uniformly infectious disease (viremia) at the time of donation or whether these two recipients were immune to HCV infection as a result of earlier exposure to the agent remains to be elucidated. In addition, although the samples from these two donors were also positive on RIBA, the possibility of a false positive result cannot be discarded, since the confirmatory power of this test has not been established. Finally, the observed 4 percent base-line (pretransfusion) prevalence of anti-HCV antibody in the recipients did not appear to be associated with any specific risk factor inherent in the heart surgery; only 2 of the 11 carrier recipients had received a previous transfusion or had undergone major surgery before entering the study. It is noteworthy, however, that all but one of these patients were 60 or older (range, 60 to 71) and represented 6.5 percent of the study population in this age group (137 recipients). This age-adjusted prevalence of base-line HCV infection was three times higher than that observed among 506 blood donors matched for age and sex who were tested (6.5 vs. 2.1 percent, P = 0.019) (data not shown). The reason for this difference remains to be determined.
Considering the above-mentioned figures, the prevalence of HCV events (27 cases of hepatitis and 2 seroconversions) in the population of susceptible recipients (269 anti-HCV—negative recipients at enrollment) was close to 11 percent, which represents a more accurate estimate of the current risk of HCV infection by blood transfusion in our area.
Although the presence of a donor positive for anti-HCV antibody was the only variable independently associated with a high risk of hepatitis in recipients, our analysis of the independent contribution of an elevated level of alanine aminotransferase in donor blood was limited by the fact that only 147 complete sets of donors had been tested for this marker. Therefore, the potential value of screening for high levels of alanine aminotransferase to reduce residual cases of transfusion-associated hepatitis after the implementation of anti-HCV screening should be further evaluated.
In summary, the results of our study suggest that screening blood donors for anti-HCV antibody may prevent close to 60 percent of the cases of transfusion-associated hepatitis, and that after the implementation of such screening most residual cases of hepatitis will be due to HCV transmitted by persistently seronegative donors.
Supported in part by grants from the Comision Interministerial de Ciencia y Tecnología (88/0221) and the Fondo de Investigaciones Sanitarias de la Seguridad Social (89/0399).
We are indebted to the medical, technical, and nursing staffs of the Blood Bank, Institut Catala de la Salut, and Cardiac Surgery Unit and to the technical and outpatient nursing staffs of the Department of Biochemistry, Hospital General Vail d'Hebron; to A. Soler for excellent technical assistance; and to Ortho Diagnostic Systems for kindly providing the anti-HCV test kits.
Source Information
From the Liver Unit (J.I.E., A.G., L.V., J.C.L.-T., D.L., R.E., J.G.), Blood Bank (J.M.H., C.S.), and Clinical Pharmacology Unit (X.V.), Department of Internal Medicine, Hospital General Universitari Vail d'Hebron; and the Blood Bank, Institut Catala de la Salut (C.M.-V.), Universitat Autònoma de Barcelona, both in Barcelona, Spain. Address reprint requests to Dr. Guardia at the Department of Internal Medicine, Hospital General Vall d'Hebron, Po Vail d'Hebron s/n., 08035 Barcelona, Spain.
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