Abstract
OBJECTIVE:
To determine the prevalence of exposure to cytomegalovirus (CMV), Toxoplasma gondii, syphilis, hepatitis B virus (HBV) and hepatitis C virus (HCV) in a large, well characterized, regional population presenting for human immunodeficency virus (HIV) care.
DESIGN:
Demographic and serological data compiled prospectively in a relational database used for routine patient care. Results were analyzed for statistically significant trends within demographic subpopulations known to be at risk of such infections.
PATIENTS AND SETTING:
A total of 1274 persons with documented HIV infection in southern Alberta have sought medical care since 1985. Serological status to CMV, T gondii, syphilis, HBV and HCV infections were routinely requested as part of the initial assessment. All patients with serological results available were included in the analysis.
RESULTS:
CMV infection was found in 84.1% of patients. A lower prevalence of CMV infection in those under 30 yeasr old (P<0.001), intravenous drug users (IVDUs) (P=0.001) and in patients with transfusion-acquired HIV (P<0.001) was seen. T gondii seropositivity was found in 10.6% of patients, with an increased risk of seropositivity in those born outside of Canada (P<0.001). Syphilis seropositivity was present in 5.1% of patients, with a higher prevalence in gay males (P=0.1). HBV carrier status was noted in 8.0% of patients, with males having an increased risk (P=0.025). Since 1990, there has been a 17.6% prevalence of HCV, predominantly in IVDUs (P<0.001).
CONCLUSION:
Seroprevalence to common pathogens in HIV disease varies significantly among subpopulations, necessitating individual testing.
Keywords: Education, Epidemiology, Opportunistic infections, Prevention, Risk factors
Abstract
OBJECTIF :
Déterminer la prévalence de l’exposition au cytomégalovirus (CMV), à Toxoplasma gondii, à la syphilis, à l’hépatite B et à l’hépatite C dans une population régionale bien caractérisée et nombreuse, nécessitant des soins pour l’infection au virus de l’immunodéficience humaine.
MODÈLE :
Des données démographiques et sérologiques ont été compilées de façon prospective dans une base de données relationnelle utilisée pour la prestation des soins standard. Les résultats ont été analysés pour déceler les tendances statistiquement significatives à l’intérieur d’une sous-population démographique exposée à un risque à l’égard de ce type d’infection.
PATIENTS ET CONTEXTE :
En tout, 1 274 personnes vivant dans le Sud de l’Alberta et présentant une infection au VIH documentée ont consulté depuis 1985. Le statut sérologique à l’égard du CMV, de T. gondii, de la syphilis, du HBV et du HCV a été demandé d’emblée dans le cadre de l’évaluation initiale. Tous les patients dont les résultats sérologiques étaient disponibles ont été inclus dans l’analyse.
RÉSULTATS :
On a identifié l’infection à CMV chez 84,1 % des patients, avec une prévalence moindre de l’infection à CMV chez ceux de moins de 30 ans (P < 0,001), chez les toxicomanes (P = 0,001) et chez les patients ayant contracté le VIH lors d’une transfusion (P < 0,001). La séropositivité à l’égard de T. gondii a été observée chez 12,6 % des patients, avec risque accru de séropositivité chez les sujets nés à l’extérieur du Canada (P < 0,001). La séropositivité à l’égard de la syphilis a été observée chez 5,1 % des patients, avec une prévalence plus forte chez les hommes gais (P = 0,1). Le statut de porteur du HBV a été noté chez 8,0 % des patients, les hommes présentant un risque accru (P = 0,025). Depuis 1990, on a observé une prévalence de 17,6 % des cas de HCV surtout chez les toxicomanes (P < 0,001).
CONCLUSION :
La séroprévalence à l’égard d’organismes pathogènes courants dans la maladie au VIH varie significativement selon les sous-populations, ce qui nécessite l’application de tests individuels.
Aggressive attempts to prevent reactivation of latent opportunistic infections, treat concurrent infections and reduce susceptibility to new infections are the cornerstones in the comprehensive care for the individual infected with human immunodeficiency virus (HIV) (1). Despite this approach, there is limited information published on the prevalence of, or susceptibility to, many of the common infections in newly diagnosed HIV-infected patients. Many social, medical and geographic variables may determine the exposure to major pathogens such as cytomegalovirus (CMV), Toxoplasma gondii, Treponema pallidum (syphilis), hepatitis B virus (HBV) and hepatitis C virus (HCV) (2–5). For the community, data on the prevalence of such infections are important in guiding public health policies and interventions. For the individual with HIV infection and his or her clinician, these data are critical to optimizing care. The purpose of this study was to determine the prevalence of previous exposure to these five pathogens in a large, well-defined, regional, HIV-infected population presenting for care over a 12-year period.
PATIENTS AND METHODS
Study population:
The Southern Alberta HIV Clinic has provided care to 1274 patients residing in southern Alberta with documented HIV infection from November 1985 to May 1997. As part of the initial assessment of all HIV-infected patients, serological testing for CMV infection, T gondii infection, syphilis, HBV and, since 1990, HCV infection is routinely ordered. The results of these tests were entered into a computerized relational database that is used to facillate routine care as well as for administrative and epidemiological purposes. Patients missing either certain serological results or specific demographic information were considered unevaluable and excluded from the statistical analysis of that group.
Serology:
CMV serology was determined to be positive on the basis of the presence of immunoglobulin (Ig) G antibodies to CMV with the Enzygnost Enzyme Immunoassay (EIA, Behring Diagnostics Inc, California). Until 1994, toxoplasma serology was determined to be positive if IgG antibodies to T gondii were present at a titre greater than 1/64 using the Organon Teknika EIA Kit (North Carolina) and, after 1994,using the EIA Platella kit (Sanofi, Paris, France). Syphilis serology was determined to be positive on the basis of a positive rapid plasma reagin test confirmed by a positive micro hemagglutination assay or a positive FTAb test (Miles Laboratories, Indiana). Hepatitis B serology was deemed to be positive by the presence of hepatitis B surface antigen (HBsAg) in the blood using an enzyme immunoassay (EIA) test up to 1989 (Abbott Laboratories) and the Uniform Two kit enzyme linked immunoassay since 1989 (ELISA, Organon Teknika). Hepatitis C serology was deemed to be positive by the presence of IgG to hepatitis C in blood as determined by the Ortho-Chiron recombinant immunoblot antibody assay, first generation from 1990 to 1992, second generation 1993 to 1994 and third generation from 1995 onwards (RIBA, Chiron Corporation, California). Where patietns had more than one test result available, the serological report obtained at the time of initial assessment was included in the study.
Statistical methods:
Seroprevalence of each of the five pathogens was determined for the entire population and then compared among sex, country of birth, ethnicity, year of first visit, age at first visit and risk factor for acquisition of HIV. The relationship between seropositivity and the group being analyzed was determined using a one-tailed χ2 test, or Fisher’s exact t test where applicable with small sample sizes, and a statistical significance level of 0.05.
RESULTS
CMV:
For 1058 of 1274 patients, CMV serology results were available (Table 1). Eight hundred and ninety of 1058 patients (84.1%) had positive serology to CMV infection. There was no temporal change in seropositivity between patients with HIV diagnosed between 1985 and 1990 and those diagnosed in 1991 or later. There was no statistically significant difference in seroprevalence between the sexes. Non-Caucasians had a slightly higher risk of being seropositive than Caucasians (P=0.01). Patients born outside of Canada showed a statistically significant increased risk of being seropositive for CMV infection compared with those born within Canada (P=0.001). Patients who acquired HIV through receipt of blood or blood products had the lowest serological prevalence to CMV infection, with 46.7% being serologically positive; in comparison, 88.2% of homosexual males were serologically positive (P<0.001). Intravenous drug users (IVDUs) and patients with other risk factors for the acquisition of HIV infection also showed a statistically significant decrease in risk for CMV seropositivity (P=0.001). The likelihood of being serologically positive to CMV infection increased with age at first visit, in that 76.6% of patients with HIV infection younger than 30 years of age were positive in contrast with 92.6% of patients aged 45 years or older (P<0.001).
TABLE 1.
Seroprevalence of cytomegalovirus in a regional human immunodeficiency virus seropositive population
| Category | Number (%) tested negative | Number (%) tested positive | P |
|---|---|---|---|
| Total population | 168 (15.9) | 890 (84.1) | |
| Sex | |||
| Male | 150 (15.3) | 828 (84.7) | 0.10 |
| Female | 18 (22.5) | 62 (77.5) | |
| Country of birth | |||
| Canada | 126 (17.3) | 602 (82.7) | 0.001 |
| Outside Canada | 8 (6.2) | 121 (93.8) | |
| Unknown | 34 | 167 | |
| Ethnicity | |||
| Caucasian | 149 (17.0) | 729 (83.0) | 0.01 |
| Other | 12 (8.6) | 128 (91.4) | |
| Unknown | 7 | 33 | |
| First visit | |||
| 1985 to 1990 | 57 (15.2) | 319 (84.8) | 0.60 |
| 1991 to 1996 | 111 (16.3) | 571 (83.7) | |
| Age (years) | |||
| Younger than 30 | 87 (23.4) | 285 (76.6) | <0.001 |
| 30 to 45 | 72 (12.7) | 493 (87.3) | 0.10 |
| Older than 45 | 9 (7.4) | 112 (92.6) | 0.01 |
| Risk factor | |||
| Men who have sex with men | 98 (11.8) | 736 (88.2) | 0.001 |
| Intravenous drug users | 23 (28.0) | 59 (72.0) | 0.001 |
| Blood product recipients | 16 (53.3) | 14 (46.7) | <0.001 |
| Other | 31 (27.2) | 83 (72.8) | 0.001 |
T gondii:
For 1074 of 1274 patients, toxoplasma serology results were available (Table 2). One hundred and fourteen of 1074 patients (10.6%) showed serological evidence for T gondii infection. Year of presentation, sex, ethnic background and risks for HIV acquisition did not show statistically significant differences among the groups analyzed. Country of birth was statistically significant; 25.4% of patients born outside Canada were serologically positive to T gondii infection in contrast with 7.8% of those born within Canada (P<0.001). The probability of being seropositive to T gondii was significantly higher for patients over the age of 45 years (P=0.001).
TABLE 2.
Seroprevalence of Toxoplasma gondii in a regional human immunodeficiency virus seropositive population
| Category | Number (%) tested negative | Number (%) tested positive | P |
|---|---|---|---|
| Total population | 960 (89.4) | 114 (10.6) | |
| Sex | |||
| Male | 887 (89.4) | 105 (10.6) | 0.99 |
| Female | 73 (89.0) | 9 (11.0) | |
| Country of birth | |||
| Canada | 683 (92.2) | 58 (7.8) | <0.001 |
| Outside Canada | 94 (74.6) | 32 (25.4) | |
| Unknown | 183 | 24 | |
| Ethnicity | |||
| Caucasian | 809 (90.0) | 90 (10.0) | 0.06 |
| Other | 113 (85.0) | 20 (15.0) | |
| Unknown | 37 | 4 | |
| First visit | |||
| 1985 to 1990 | 362 (88.1) | 49 (11.9) | 0.30 |
| 1991 to 1996 | 598 (90.2) | 65 (9.8) | |
| Age (years) | |||
| Younger than 30 | 337 (91.3) | 32 (8.7) | 0.25 |
| 30 to 45 | 523 (90.2) | 57 (9.8) | 0.70 |
| Older than 45 | 100 (80.0) | 25 (20.0) | 0.001 |
| Risk factor | |||
| Men who have sex with men | 756 (89.4) | 90 (10.6) | 0.99 |
| Intravenous drug users | 78 (95.1) | 4 (4.9) | 0.06 |
| Blood product recipients | 30 (90.9) | 3 (9.1) | 0.99 |
| Other | 96 (93.2) | 7 (6.8) | 0.25 |
Syphilis:
Syphilis serology was available for 1092 of 1274 patients (Table 3). Positive results were obtained in 56 of 1092 (5.1%) of those tested. There was no statistically significant difference in group analysis by ethnicity, country of birth or in year of presentation for care. Females had a slightly lower risk of being seropositive to syphilis than males (P=0.05). Seroprevalence was higher in patients whose risk factor for acquiring HIV infection was homosexuality (6.3%) compared with intravenous drug use (3.8%), but these numbers failed to reach statistical significance (P=0.1). Patients younger than age 30 years had a significantly lower rate of seropositivity (2.4%, P=0.01) than patients over age 45 years (8.7%, P=0.025).
TABLE 3.
Seroprevalence of syphilis in a regional human immunodeficiency virus seropositive population
| Category | Number (%) tested negative | Number (%) tested positive | P |
|---|---|---|---|
| Total population | 1036 (94.9) | 56 (5.1) | |
| Sex | |||
| Male | 957 (94.6) | 55 (5.4) | 0.05 |
| Female | 79 (98.8) | 1 (1.2) | |
| Country of birth | |||
| Canada | 702 (95.6) | 32 (4.4) | 0.25 |
| Outside Canada | 119 (93.0) | 9 (7.0) | |
| Unknown | 115 | 15 | |
| Ethnicity | |||
| Caucasian | 871 (93.7) | 49 (6.3) | 0.75 |
| Other | 129 (94.9) | 7 (5.1) | |
| Unknown | 36 | 0 | |
| First visit | |||
| 1985 to 1990 | 385 (94.8) | 21 (5.2) | 0.99 |
| 1991 to 1996 | 651 (94.9) | 35 (5.1) | |
| Age (years) | |||
| Younger than 30 | 369 (97.6) | 9 (2.4) | 0.025 |
| 30 to 45 | 552 (93.9) | 36 (6.1) | 0.25 |
| Older than 45 | 115 (91.3) | 11 (8.7) | 0.03 |
| Risk factor | |||
| Men who have sex with men | 814 (93.7) | 55 (6.3) | 0.10 |
| Intravenous drug users | 75 (96.2) | 3 (3.8) | 0.80 |
| Blood product recipients | 26 (92.9) | 2 (7.1) | 0.30 |
| Other | 115 (98.3) | 2 (1.7) | 0.10 |
HBV:
HBSAg serology results, signifying HBV carrier status, were available for 1031 of 1274 patients at the clinic, of which 82 (8.0%) were positive (Table 4). Male patients had a significantly higher incidence of seropositivity than females (P=0.025). There was no difference in seropositivity by year of presentation, patient age, country of birth, ethnicity or risk for HIV acquisition obtained through group analysis.
TABLE 4.
Seroprevalence of hepatitis B in a regional human immunodeficiency virus seropositive population
| Category | Number (%) tested negative | Number (%) tested positive | P |
|---|---|---|---|
| Total population | 949 (92.0) | 82 (8.0) | |
| Sex | |||
| Male | 878 (90.6) | 81 (9.4) | 0.025 |
| Female | 71 (98.6) | 1 (1.4) | |
| Country of birth | |||
| Canada | 614 (91.9) | 54 (8.1) | 0.90 |
| Outside Canada | 112 (91.8) | 10 (8.2) | |
| Unknown | 223 | 18 | |
| Ethnicity | |||
| Caucasian | 800 (91.4) | 75 (8.6) | 0.75 |
| Other | 107 (93.9) | 7 (6.1) | |
| Unknown | 42 | 0 | |
| First visit | |||
| 1985 to 1990 | 401 (91.6) | 37 (8.4) | 0.80 |
| 1991 to 1996 | 548 (92.4) | 45 (7.6) | |
| Age (years) | |||
| Younger than 30 | 348 (92.8) | 27 (7.2) | 0.60 |
| 30 to 45 | 492 (90.9) | 49 (9.1) | 0.75 |
| Older than 45 | 109 (94.8) | 6 (5.2) | 0.30 |
| Risk factor | |||
| Men who have sex with men | 762 (91.3) | 73 (8.7) | 0.50 |
| Intravenous drug users | 56 (93.3) | 4 (6.7) | 0.60 |
| Blood product recipients | 29 (96.7) | 1 (3.3) | 0.50 |
| Other | 102 (96.2) | 4 (3.8) | 0.10 |
HCV:
Two hundred and fifty-six patients received hepatitis C serology testing since its introduction in 1990 (Table 5). Of these, 45 (17.6%) were positive. Risk factor for acquiring HIV infection was highly significant. Only 10 patients (6.0%) whose risk factor was homosexuality had positive hepatitis C serology compared with 31 IVDUs (70.5%) (P<0.001). Patients born outside of Canada showed a statistically significant lower risk for positive hepatitis C serology compared with those born in Canada (P=0.025), although the small numbers of patients born outside Canada suggest interpreting this result with caution. Patients whose ethnicity was not Caucasian showed a statistically significant higher risk of positive serology than Caucasians (P=0.005). A highly significant increase in risk for positive hepatitis C serology was seen in patients younger than 30 year (27.7%) compared with those above 45 years of age (6.3%, P=0.03). There was no significant difference between sex.
TABLE 5.
Seroprevalence of hepatitis C in a regional human immunodeficiency virus seropositive population
| Category | Number (%) tested negative | Number (%) tested positive | P |
|---|---|---|---|
| Total population | 211 (82.4) | 45 (17.6) | |
| Sex | |||
| Male | 192 (83.8) | 37 (16.2) | 0.10 |
| Female | 19 (70.4) | 8 (29.6) | |
| Country of birth | |||
| Canada | 173 (79.7) | 44 (20.3) | 0.025 |
| Outside Canada | 38 (95.0) | 2 (5.0) | |
| Ethnicity | |||
| Caucasian | 180 (85.3) | 31 (14.7) | 0.01 |
| Other | 31 (68.9) | 14 (31.1) | |
| First visit | |||
| 1985 to 1990 | 27 (100) | 0 (0) | 0.01 |
| 1991 to 1996 | 184 (81.1) | 43 (18.9) | |
| Age (years) | |||
| Younger than 30 | 47 (72.3) | 18 (27.7) | 0.03 |
| 30 to 45 | 128 (83.7) | 25 (16.3) | 0.75 |
| Older than 45 | 36 (93.7) | 2 (6.3) | 0.03 |
| Risk factor | |||
| Men who have sex with men | 157 (94.0) | 10 (6.0) | <0.001 |
| Intravenous drug users | 13 (29.5) | 31 (70.5) | <0.001 |
| Blood product recipients | 6 (85.7) | 1 (14.3) | 0.99 |
| Other | 35 (92.1) | 3 (7.9) | 0.10 |
DISCUSSION
Knowledge of the prevalence of exposure to various pathogens in an HIV-positive population is important for both the individual and the community (1). For the individual, it allows appropriate preventative, prophylactic and therapeutic regimens to be implemented. For the community, it allows for the overlap of different diseases to be monitored, thus opening the opportunity for prevention of exposure in susceptible populations.
CMV is a ubiquitous and endemic pathogen transmitted by close physical contact with body fluid from an infected person (2). Its prevalence is related to socioeconomic status and geographical location, ranging from 13% to 60% in areas of the United States, to 40% in Canada and Europe, and nearly 100% in Africa and the far east (6). The rate of infection within our HIV seropositive population is high at 84.1%. We did not see a difference between males and females, which contradicts the findings of some previous studies. Previous studies support our findings in that ethnic background and country of birth were found to influence the seroprevalence of CMV (7,8). We also saw the frequency of positive serology for CMV increase with age. IVDUs, and blood and blood product recipients also showed a relatively decreased risk of being seropositive for CMV, which has not been previously noted in HIV-infected populations. Homosexual males have a high prevalence of CMV, and made up the majority of the population studied. HIV-infected individuals within low risk groupings should receive advice on how to reduce their risk of CMV acquisition, while individuals in the high risk groups might consider prophylaxis against reactivation of the pathogen.
Seroprevalence of T gondii, which is most commonly acquired by ingestion of oocytes or viable cysts from feces or food, is influenced by geographic, climatic, ethnic and socioeconomic factors (3). The prevalence of positive T gondii serology in the general population varies from 13% to 40% among regions in Canada (9,10). In Canada, there is a documented increase in positivity of 2.5 times for those born outside of the country (9). Age, but not sex, has been identified as a significant risk factor, but it has recently been suggested that being a non-Caucasian male may also be a risk factor (3,11,12). The prevalence of positive T gondii serology among HIV-infected patients also varies greatly worldwide at 16% and higher in the United States, 27% in the United Kingdom, 59% in France and up to 96% in areas of western Europe and Africa (11–14). We found a low overall prevalence of 10.6%, not related to sex or risk of HIV acquisition. We saw a statistically significant high prevalence in patients born outside of Canada. An increase in positivity as age increased, that reached statistically significant values for patients over age 45 years, was observed. The low prevalence of infection and the use of prophylactic regimens explains the very low incidence of T gondii disease in our patient population, with only 14 cases seen in 1274 patients over 12 years.
Homosexual males have accounted for 46% to 58% of all syphilis cases in North America since 1990 (4,15,16). The seroprevalence of syphilis in HIV-infected patients (28% to 31%) has been reported to be as high as five to seven times that of HIV-negative individuals (4% to 6%) in some parts of the United States (4,15,16). The rate of positive syphilis serology in our HIV-infected population was found to be low (5.1%) and similar to the documented seroprevalence of HIV-negative individuals. This suggests that other factors besides HIV infection contribute to syphilis exposure. Positivity was lower in patients under age 30 years, and higher in patients over age 45 years, supporting the previous belief that the chance of exposure to this pathogen increases with age. No temporal change in the seroprevalence of syphilis over the past 12 years was noted in our population.
Transmission of HBV commonly occurs through sexual contact and intravenous drug use, and rarely through blood transfusion (17,5). An increase in prevalence is seen with increasing age, although overall prevalence varies within different socioeconomic and geographic groupings (5). One of the main risk factors identified for acquisition of HBV is the endemic rate of HBV within one’s country of origin (17). We found no difference in seropositivity among country of birth; however most of our patients born outside of Canada came from countries with a low prevalence or prevalence equivalent to that in Canada. Some studies have shown that while the seroprevalence of HBV may be around 20% for HIV-negative patients, for the HIV-positive population it could be as high as 70% (5). This is much higher than our results demonstrated, with an overall positive serology rate within our population of only 8%. No group in our analysis had a significantly increased risk of positive serology over the total population, although a significantly lower percentage of females had positive serology than males.
Intravenous needle sharing and blood transfusions have been identified as important vehicles for HCV transmission, with seropositivity as high as 95% in these groups (5,18,19). The seroprevalence in frequent recipients of blood or blood products has been measured as high as 87% (18,20). Our study demonstrated a low seroprevalence in this group (14.3%) not significantly different from our whole population. IVDUs were identified as the largest proportion of seropositive patients in our study (70%). Sexual spread of HCV does occurs infrequently, with negligible incidence among spouses of HCV seropositive individuals (18). Our results support other published results in that gay males had a low seroprevalence of infection (6.0%). Positive HCV serology has been measured at 8% in persons attending sexually transmitted disease clinics in the United States (18). The prevalence and trends of HCV infection in the general population has been documented as being similar between HIV-positive (9.2%) and HIV-negative (7.9%) people (5). The results obtained for our population follows these general trends.
CONCLUSIONS
The results obtained from our study provide a detailed serological profile of our past and present clinic population, and explain the spectrum of opportunistic infections seen in our population over the past 12 years. General trends in prevalence that were previously reported in non-HIV-infected populations were demonstrated with some unique characteristics. This knowledge aids the development of strategies to reduce the frequency of opportunistic infections in the future and suggests possible interventions when serology results are unavailable.
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