Epidemiology of adult and adolescent HIV infection in Israel: a country of immigration

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ORIGINAL RESEARCH ARTICLE

Epidemiology of adult and adolescent HIV

infection in Israel: a country of immigration

D Chemtob

MD MPH1

and

Z Grossman

PhD2

1Department of Tuberculosis and AIDS, Ministry of Health, POB 1176, Jerusalem; 2HIV Reference Laboratory, Central Virology Laboratory, PHL, MOH, Sheba Medical Centre,

Tel Hashomer, Israel

Summary: In Israel, the caseload and main modes of transmission have changed dramatically since 1991 after mass immigration from countries with generalized HIV epidemics. The previous annual average (of 60 new cases) has almost quadrupled, and 68% are among heterosexuals (compared with 11.6% before). We verified all HIV/AIDS cases ever documented, redefined (according to UNAIDS/WHO definitions) and analysed those aged 13+. Between 1980–2000, HIV and AIDS were diagnosed, respectively, in 2204 and 682 adults and adolescents (cumulative HIV infection rate¼61/100 000). Of these, 65.2% are male (mean age 35.0 years old; SD¼11.0), 31.5% female (mean age 31.4 years old; SD¼10.5) (and 3.3%, sex unknown). The main modes of HIV transmission were heterosexual (45%), MSM (16.9%) and IDUs (11.5%). Prevention measures must be strengthened, if the currently low-level of HIV epidemic among the Israeli general population is to be sustained.

Keywords: HIV infection, epidemiology, immigrants, heterosexuals, Israel

Introduction

The first case of AIDS in Israel, a country of immigration with several unique characteristics of the HIV infection was (retrospectively) diagnosed as having occurred in 1980. By the end of 2000, 682 cases of AIDS and 2204 HIV-positive individuals of 13 years and over were diagnosed. In this article, we analyse the epidemiology of adult and adolescent HIV infection in Israel since the last summary, which covered the years 1980–921. We

discuss the implications of this analysis for public health policy as recommended in the recent guide-lines from UNAIDS/WHO2.

Sources of data and updating methods

The data relate only to HIV/AIDS cases among adults and adolescents ever notified to the Israeli Ministry of Health (MOH).

Source of data

Clinicians and laboratories have had to report AIDS since 1983 and HIV infection since 1999, but HIV has, in fact, been reported since 1986. Cases diagnosed before have been included in the National Register since 1986. HIV/AIDS case investigation is done in the seven regional AIDS

centres (each one including a clinic and a laboratory) and/or by 15 local District Health Offices (DHO) who notify the AIDS department in the MOH where the data are recorded in the National Register.

Enzyme linked immunosorbent assay (ELISA) testing for HIV is available on request, free of charge. All donated blood and organs have been screened for HIV since 1986. In addition, every new immigrant (aged nine years and more) from Ethiopia is screened for HIV on arrival (since 1991). Systematic screenings are performed in jails and for some military recruits. The regional laboratories and the Blood Services perform ELISA for HIV antibodies and forward all samples found to be positive twice, for Western blot (WB) to the national Reference Laboratory. Each confirmed case is reported back to the medical source of specimen, to the DHO and to the AIDS Depart-ment.

Updating methods and classifications

We retrospectively matched all HIV/AIDS cases directly with all regional AIDS centres, DHOs and with the Reference Laboratory and re-defined them according to the latest WHO definitions3,4. We

redefined the heterosexual cases according to the recent UNAIDS/WHO guidelines for second generation surveillance for HIV infection2

differ-entiating between three different epidemic states; low-level, concentrated, and generalized. We also

691 Correspondence to: Dr Daniel Chemtob

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reviewed all cases notified in 1997–2000 according to the instructions of the pilot phase of the European HIV reporting system5, and analysed

the impact of our active case finding (ACF) policy. We defined place of infection by analysing the interval between immigration (or entrance for tourists) and HIV notification. We classified im-migrants (or tourists) as follows: every (Israeli citizen) Ethiopian immigrant, who was notified as HIV positive in the same year or in the calendar year after his/her arrival in Israel, was considered to be infected abroad (these immigrants underwent ACF at arrival since 1991). After this period, we considered all notified HIV cases among this population as being infected in Israel. For other immigrants our analysis further differentiated between Israeli citizens (usually from countries with low or concentrated levels of HIV) and between non-Israeli citizens (mainly from countries with generalized HIV). They were considered as being infected abroad when they were notified for HIV before the third year after their arrival, and considered being infected in Israel when notified following this third year.

This report is based upon notifications received in the AIDS Department up to 30 June 2001.

Results

Some 160–200 thousand ELISA tests are done each year (for a total average population of 6.29 million individuals in 2000)6. Some 200 000-blood

dona-tions are also tested every year (Head of the Blood Services, Shinar E. personal communication).

Between 1980–2000, AIDS and HIV-positivity were diagnosed among adults/adolescents in 682 and 2204 cases, respectively (cumulative HIV infection rate is 61/100 000). Of these, 1881 (65.2%) are males, 910 (31.5%) females (and 95 — 3.3% — gender unknown). Average ages for males and females are respectively 35.0 years old (SD¼11.0) and 31.4 years old (SD¼10.5).

The annual distribution of new HIV/AIDS cases (according to WHO modes of transmission categories) is shown in Figure 1.

A shift occurred in 1991, mainly due to mass immigration from countries with generalized HIV epidemics. Before 1991, the annual average number of new persons living with HIV (PLWHIV) was relatively low (61); mainly male (86.4%) and only 11.6% was among heterosexuals. Since 1991, the annual average has almost quadrupled and 68% were among heterosexuals (Table 1).

Comparing 1981–1990 to 1991–2000, there were major changes in the primary modes of HIV transmission for both HIV/and AIDS cases (Table 1). Unprotected sexual relations among men who have sex with men (MSM) decreased from 39.3% to 11% of all PLWHIV cases and from 45.4% to 18.4% of all male PLWHIV cases. Injecting drug users (IDUs) decreased from 25.7% to 8.7%. Transfusion of infected blood products and/or by transplanta-tion of infected organs decreased from 13.1% to 0.6%. Heterosexual relationship increased drama-tically from 11.6% to 68% of total cases. Unknown mode of transmission was stable; 10.3% compared with 11.7%.

The mode of transmission and the presumed place of infection are shown in Tables 2 and 3. For the overall period (1980–2000), the primary modes of transmission among AIDS cases were (1)

Hetero¼Heterosexual transmission; MSM¼men who have sex with men; IDU¼Intravenous drug user; Haemophilia & blood¼transmission by transfusion of infected blood products and/or by infected organs

Figure 1. AIDS/HIV new cases, by year of notification and by modes of transmission categories, Israel 1980–2000.

Table 1. Dramatic changes in the total number, gender distribution and mode of HIV transmission of the HIV/AIDS cases in Israel, when comparing two notification periods, Israel 1981–2000*

1981–1990 1991–2000

Annual average no. of new cases

No. of cases

% of heterosexual

Annual average no. of new cases

No. of cases % of heterosexual Total no of HIV/AIDS cases Male 53 528 6.2 135 1352 58.9 1880 Female 7 71 53.5 84 839 86.8 910 Unknown gender 1 12 – 8 83 25.3{ 95 Total 61 611 11.6 227 2274 68 2885*

*Only one (male) case was reported for the year 1980 and therefore, in order to prevent a biased analysis, this year was excluded from this table

{Despite the fact that the gender was not notified, data on country of origin existed, and allowed us to classify these cases as originating from countries with HIV generalized

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heterosexual relationship among persons immi-grating from generalized HIV epidemic countries (33.0%), and (2) unprotected sexual relations among MSM (28.6% of all AIDS cases but 36.4% of all male AIDS cases; Table 2). The presumed place of infection was considered to be abroad for more than half of AIDS and HIV cases (50.3% and 56.9% respectively; Tables 2 and 3).

For HIV infection, the main known mode of transmission was heterosexual relationship among persons immigrating from countries with general-ized HIV epidemics (48.8%), followed by undeter-mined transmission category (13.6%) and then by unprotected sexual relations among MSM (13.4% of all HIV cases but 21.9% of male HIV cases; Table 3).

Concerning IDU alone and both MSM and IDUs, they represent 15.1% and 11.5% of all AIDS and HIV cases, respectively. Male/Female ratio was 4.3, and the average age at HIV notification was 30.9 years old (SD¼7.0). Since 1997, there has been a significant increase in new HIV/AIDS cases among IDUs (from an average of 10 new cases per year for the period 1992–96 to an average of 32 per year for the period 1997–2000). Moreover, some 79.5% of the IDUs were presumed to have been infected abroad with HIV for the period 1997–2000, compared with 51.7% of IDUs in the period 1980–96. In the last four years, most of those infected abroad (86.6%) came from the Former Soviet Union (FSU).

Concerning the MSM transmission category, the absolute number of new cases (an annual average

Table 2. Notified AIDS patients by sex, mode of transmission and presumed place of infection, Israel 1980–2000 Total

Cumulative number Place of infection (%)

Transmission category Male Female Total Israel Abroad UNK Died (%) Left Israel (%)

1. MSM 195 195 57.9 40.5 1.6 76.9 5.1 2. IDU 74 16 90 58.9 41.1 0 67.8 2.2 3. MSM+IDU 13 13 23 77 0 84.6 7.7 4. Haemophilia 37 37 97.3 2.7 0 97.3 0 5. Other blood 10 7 17 82.3 17.7 0 88.2 0 6. Heterosexual contacts 6.1 OGE 142 83 225 17.8 82.2 0 52.9 1.8

6.2 Partners from 1–5 categories 1 19 20 85 15 0 60 0

6.3 SWOGE 1 1 100 0 100 0

6.4 Sex with HIV not known as 6.1–6.3 7 7 14 85.7 14.3 0 71.4 0

6.5 Source undetermined 28 12 40 72.5 27.5 0 62.5 2.5

7. Other/undetermined 29 1 30 60 36.7 3.3 76.7 3.3

Total 536 146 682 49.1 50.3 0.6 67.9 2.8

MSM¼men who have sex with men; IDU¼intravenous drug user; UNK¼unknown; OGE¼originating from a country with a generalized HIV epidemic; SWOGE¼sex with a person originating from or living in a country with a generalized HIV epidemic

Table 3.Notified HIV-positive persons not known to have progressed to AIDS, by sex, mode of transmission and presumed place of infection, Israel 1985–2000

Total

Cumulative number Place of infection (%)

Transmission category Male Female UNK Total Israel Abroad UNK Died (%) Left Israel (%)

1. MSM 295 – – 295 65.4 20.0 14.6 6.1 5.0 2. IDU 186 49 7 242 43.0 48.8 8.2 13.6 5.4 3. MSM+IDU 11 – – 11 72.7 18.2 9.1 36.4 4. Haemophilia 34 – 34 100 0 0 32.3 5. Other blood 5 1 6 66.6 33.4 83.3 6. Heterosexual contacts 6.1 OGE 544 516 16 1076 25.1 74.2 0.7 3 2.5

6.2 Partners from 1–5 categories 2 27 29 69 31 0 10.3

6.3 SWOGE 1 6 7 100 0 0

6.4 Sex with HIV not known as 6.1–6.3 19 26 45 75.6 24.4 0 4.4

6.5 Source undetermined 86 69 5 160 48.1 48.1 3.8 2.5

7. Other/undetermined 162 70 67 299 19.7 56.9 23.4 4.3 4.3

Total 1345 764 95 2204 36.8 56.5 6.7 5.5 3.5

MSM¼men who have sex with men; IDU¼intravenous drug user; UNK¼Unknown; OGE¼originating from a country with a generalized HIV epidemic; SWOGE¼sex with a person originating from or living in a country with a generalized HIV epidemic

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of less than 25 new cases in the period 1991–2000) has been stable in the last years (Figure 1), but rates have decreased considering the increase in general population in the last years.

In Table 4, the interval (in years) between immigration (or entrance for tourists) and HIV notification has been further analysed according to the definition described above. Some 70.6% of HIV/AIDS cases among (Israeli citizen) Ethiopian immigrants in Israel were considered to be infected abroad. Considering the HIV data obtained by PCF, some 44% of the Israeli citizens (almost exclusively coming from countries with low or concentrated levels of HIV epidemics) were notified less than five years after their arrival and data on entrance to Israel were missing for 91.8% of the non-Israeli citizens (mainly from countries with generalized HIV epidemics) (Table 4).

Discussion

Comparing our data to those of the WHO European Region, of which Israel is a member7,

AIDS incidence in Israel is lower than in the European Union (12.6 cases per million vs 22.5 cases per million overall, in 2000)8. HIV incidence is

also lower in Israel than in the European Union and in most of the Western European countries (e.g. 47 per million in 2000 in Israelvs57.3 in the European Union, 47.7 in Denmark, 58.7 in United Kingdom and more than 90 in Belgium in 2000)8.

Never-theless, Israeli incidence rates are significantly biased (recruitment bias) by, and heavily depen-dent, on the countries of origin of the PLWHIV. As a country of immigration, 71.2% of all PLWHIV notified in Israel were among foreign-born indivi-duals (and an additional 5.9% was among persons with non-notified country of origin or citizenship), despite the fact that only 30% of its current population (of 6.29 million) is foreign-born6.

During the last decade, Israeli citizens of Ethiopian origin, who account for only 1.3% of the total Israeli

population6, contributed to 45.4% of all the new

HIV/AIDS cases diagnosed. For the same period (1991–2000), 18.8% of HIV/AIDS cases were non-Israeli citizens. Among them, almost half were from countries with generalized HIV epidemics. Among Israeli citizens not from Ethiopia (730), 25.5% were known IDUs, of whom more than half were probably infected abroad.

Since 1991, mostly as a result from immigration from countries with generalized HIV epidemics, the number of PLWHIV in Israel, their gender distribution and also the relative proportion of their transmission categories have dramatically changed. The annual average of new cases during the second period (1991–2000) almost quadrupled compared with the first period (227 new cases vs

61 — Table 1). In women, the number of new cases increased 12-fold between these two decades. As a consequence, the mode shifted between these two periods from the ‘classical’ high-risk transmission categories (MSM and IDUs) to heterosexual transmission. Therefore, the presumed place of contracting HIV infection is very important in the understanding of HIV infection in Israel.

The rise since 1997, of HIV among IDUs from the FSU, is consistent with the emergence of an HIV epidemic in the FSU, still almost solely among IDUs9. However, in Israel, the epidemiological risk

factor for HIV transmission among IDUs remains intravenous drug injection, and not immigration from the FSU10, and therefore, we did not

recommend any systematic HIV screening of new immigrants from the FSU but rather a series of preventive measures regarding IDUs (see below).

Completeness of notification is always a concern in an analysis such as ours. The accessibility of medical services and a national health insurance plan, the small size of Israel and the concentration of most of the population in urban centres, the multiple sources of notification and our updating methods described above, lead to our assumption that the AIDS reporting fraction is close to 100%

Table 4. Interval (in years) between date of immigration (or entrance for tourists) and HIV notification*, Israel 1980–2000

No of HIV/AIDS cases (%)

Active case finding Passive case finding

Interval (in years) Israeli citizens from Ethiopia Israeli citizens Non-Israeli citizens Total No (%)

0–1 year 739 (70.6) 153 (30.4) 27 (5.4) 919 (44.7)

2 years 43 (4.1) 30 (6.0) 3 (0.6) 76 (3.7)

3–4 years 56 (5.3) 37 (7.3) 6 (1.2) 99 (4.8)

5–9 years 128 (12.2) 49 (9.7) 5 (1.0) 182 (8.9)

10 years and more 78 (7.5) 230 (45.6) 308 (15.0)

Unknown 3 (0.3) 5 (1.0) 462 (91.8) 470 (22.9)

Total 1047 (100.0) 504 (100.0) 503 (100.0) 2054 (100.0) *This does not include the 661 Israeli-born Israeli citizens, and the remaining 171 cases for which date of entrance was not obtainable due to incorrect identity card number

Note: The 88 Israeli-born individuals who have notified that they were probably exposed abroad are not included in this Table, but are registered in Tables 2 and 3

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(the main reservation is the rarity of post-mortem examination performed in Israel).

For assessing the completeness of HIV data back calculation by evaluating the percentage of ‘sur-prise AIDS cases’ (reported AIDS cases not previously registered as HIV infected) was used11.

We repeated this calculation for HIV/AIDS cases contracted in Israel or of an unknown origin. Globally 21.4% of all AIDS cases are ‘surprise AIDS cases’, and the trend was a decrease in this percentage during the last decade, from more than 40% in 1989 to 13.2% in 2000.

Nevertheless, the actual number of PLWHIV in Israel is certainly slightly higher, due to under-diagnosis. In coordination with the WHO EuroHIV we prepared an estimate of the HIV prevalence expected from our notified data12. This calculation

takes into account the dynamics of each population group, by giving a different coefficient to each component of the equation. Correct to 31 Decem-ber, 2000, we estimated 2954 PLWHIV still alive and/or in Israel vs 2205 notified, and 3645 PLWHIV (People notified with HIV/AIDS, includ-ing those who have died or left Israel) since 1980,vs

2886 notified.

Finally, we would like to address the impact of our data analysis on public health policy. In the absence of a real cure or a vaccine, primary prevention remains the most important public health concept for HIV epidemic control13.

There-fore, we propose a multifaceted approach, dealing both with the general population and with smaller groups with high risk-behaviours. We have called for a joining of forces between governmental and non-governmental organizations (NGO)14.

Preven-tion campaigns directed at the general populaPreven-tion must continue, based on extensive knowledge, attitudes and practices (KAP) studies on AIDS and other STIs (sexually transmitted infections)15.

This is important despite the fact that the general Israeli population remains at a low level of HIV epidemic state. With regard to immigrants from countries with generalized HIV epidemics, the situation in Israel concerning primary prevention is not homogeneous, partly as a result of the complexity of immigration processes in Israel analysed elsewhere16. For historical reasons, most

of immigrants to Israel are Jewish persons or Jewish descents, who immigrated according to the ‘law of Return’17 or family reunification

arrange-ments16. In addition, there are thought to be some

200,000 foreign workers in Israel today, of whom approximately half are undocumented workers16.

Among Israeli citizens from Ethiopia, culturally specific programmes were initiated in the begin-ning of the 1990s18–20, and implemented on a larger

scale since 1997 (Abramson N, personal commu-nication). Data related to ACF in this group show that since 1990, some 30% of PLWHIV notified yearly in this community are diagnosed two years or more after their immigration (Table 4), and this figure demonstrates the importance of

HIV transmission within this community, after their arrival in Israel. A prevention programme in this close-knit community was launched in 1997 and it will have to be closely evaluated to determine its effectiveness.

Concerning non-Israeli immigrants the AIDS Department is currently working with major AIDS and civil rights non-governmental organizations on a specific programme aimed at preventing AIDS in migrant workers in Israel21.

Concerning the MSM group, KAP surveys are in place (Chemtob D, personal communication) and we acted according to our findings to maintain and even reduce the transmission among MSM, at the same low level that has prevailed during the last decade (Figure 1).

Regarding IDUs there is a real fear that the prevalence rate may reach the 5% considered by UNAIDS as a ‘concentrated level’ of the HIV epidemic [2] (there are some 7000 IDUs in Israel (Mell H, personal communication); we estimate an HIV prevalence among IDUs between 1–3%). Therefore, HIV surveillance should probably focus on this sub-population, in order to identify a transmission of HIV to the general population22.

Measures including raising awareness among professionals working with drug addicted persons, expanding drug abuse treatment and counselling programmes10 and the creation of a

community-based pilot project of a syringe exchange pro-gramme23, together with prevalence serological

studies and street-based outreach conducted by peer educators are in place or planned. Finally, a recent survey among sex workers in Tel Aviv showed only one PLWHIV (out of 300 tested prostitutes) (Shohat T, personal communication, 2002), and seemed to confirm the probably very low role of prostitution in the HIV epidemic in Israel.

HIV in Israel was influenced mainly by immi-gration from countries with generalized HIV epidemics. Israel still remains at a low level of HIV epidemic but subpopulations from countries with generalized HIV epidemics and IDU deserve special attention. Mass media campaigns to raise awareness of the general public and specific interventions targeting groups with high-risk behaviours regarding HIV, must continue and even be strengthened, if the currently low level of HIV epidemic among the Israeli general population is to be sustained.

Acknowledgements: We wish to acknowledge all medical and laboratory professionals for their HIV reporting that without it, no epidemiological analysis would be possible. We are grateful to those who assisted in matching these data at the AIDS clinics, the District Health Offices, the National Reference laboratory for HIV and of course, the team at the Department of TB and AIDS, with special mention to Ms Zehuvit Wiex-elboim. Finally, we gratefully acknowledge Ms

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Niva Bessudo Manor for her assistance in prepar-ing some of the crude data, and to Dr Daniel Weiler-Ravell and Ms Beverley Damelin for their editorial assistance, three of them from the Department of TB and AIDS.

The opinions expressed in this article are those of the authors and do not purport to represent the opinions of the agencies with which they are associated.

This paper was presented in abstract form in Durban (South Africa) at the XIII International AIDS Conference, 2000.

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