Articles
Epidemiology of varicella among immigrants and non-immigrants in Quebec, Canada, before and after the introduction of childhood varicella vaccination: a retrospective cohort study

https://doi.org/10.1016/S1473-3099(20)30277-2Get rights and content

Summary

Background

Many immigrants are susceptible to varicella on arrival to Canada because of different transmission dynamics in their countries of origin and scarcity of vaccination. Universal childhood vaccination programmes decrease varicella incidence rates through herd immunity, but the accumulating number of susceptible adult immigrants could remain at risk for severe varicella. Our aim was to describe the epidemiology of varicella among immigrants and non-immigrants before and after childhood varicella vaccination.

Methods

We did a population-based, retrospective cohort study of all varicella cases in Quebec, Canada, diagnosed between 1996 and 2014 in administrative health databases linked to immigration data. Cases of varicella met diagnostic codes in the International Classification of Diseases, Ninth and Tenth Revision Canadian modifications. Cases with a co-occurring zoster diagnostic code and immigrants from Australia, New Zealand, the USA, and western European countries were excluded. Vaccination periods included pre-vaccination (1996–98), private vaccination (1999–2005), and public vaccination (2006–14). Incidence rate and comparative rate ratios were estimated using census data.

Findings

A total of 231 339 varicella cases diagnosed between Jan 1, 1996, and Dec 31, 2014, were linked to 1 115 696 immigrants who arrived between Jan 1, 1980, and Dec 31, 2014. 1444 herpes zoster cases and 1276 immigrants from Australia, western Europe, New Zealand, and the USA were excluded. Among 228 619 varicella cases, 13 315 (5·8%) occurred in immigrants. In pre-vaccination versus public vaccination periods, varicella incidence declined in immigrants by 87% (95% CI 86·6–87·9; 324·3 cases per 100 000 person-years to 40·9 cases per 100 000 person-years) and in non-immigrants by 93% (92·4–92·7; 484 cases per 100 000 person-years to 36 cases per 100 000 person-years). Mean age at diagnosis increased in both groups (15·1 vs 19·4 years in immigrants and 8·4 vs 12·0 years in non-immigrants). In the public vaccination period, immigrants younger than 50 years had higher varicella rates than non-immigrants, with relative risk ranging from 1·53 (95% CI 1·37–1·72) to 4·64 (3·90–5·53) with the highest risk in adolescents and young adults, and people from Latin America and the Caribbean (age-specific incidence rate ratio [aIRR]I-NI pre-vaccination 2·19 and post-vaccination aIRRI-NI6·07) and south Asia (aIRRI-NI pre-vaccination 3·41 and aIRRI-NI post-vaccination 4·46) and in childbearing women (15–40 years; IRRI-NI 2·48).

Interpretation

Immigrant adolescents, young adults, and women of childbearing age had higher age-standardised rates of varicella than non-immigrants, with increasing disparities following vaccine introduction. Immigrants younger than 50 years of age would benefit from targeted vaccination upon arrival to host countries.

Funding

The Canadian Institutes of Health Research and The Department of Medicine, Jewish General Hospital, Montreal, QC, Canada.

Introduction

A large proportion of adolescent and young adult immigrants from tropical countries are non-immune to varicella.1, 2, 3 This is primarily because of different transmission dynamics in hot, humid climates compared with cold climates, as well as the absence of varicella vaccination either before or after immigration.4, 5 In tropical environments varicella is transmitted less effectively and disease occurs at an older mean age (10–15 years) compared with in cold countries (about age 5 years).4, 5 Consequently, in the absence of a varicella vaccination programme, the seroprevalence of varicella in tropical countries is about 85% in individuals who are 20 years of age, whereas it is 97–100% in this population in North America and western Europe.6 Varicella is a relatively benign disease in children; however, the severity increases with age. Adults are more likely to be admitted to hospital and to die from the disease.7 Pregnant women have poorer outcomes than do other adults and can transmit varicella to their fetus or newborn infant, which can be associated with serious adverse sequelae.8

Research in context

Evidence before this study

We searched PubMed Central for reports of varicella among immigrants using the terms “Chickenpox” or “Varicella” and “Emigrants and Immigrants” or “Refugees”. The search was done on June 3, 2019, with no search date or language restrictions. A large proportion of young adult immigrants (about 15%) born in tropical climates could be susceptible to varicella upon arrival to Canada because of different transmission dynamics in their countries of origin and the absence of vaccinations. Varicella childhood vaccination has resulted in a decrease in varicella incidence rates in all age groups because of herd immunity and is cost-effective from a societal perspective. The severity of varicella increases with age and adults are more likely to be admitted to hospital and to die from varicella, and pregnant women are the individuals at the highest risk. The key potential disadvantage of childhood vaccination is shifting the age of varicella acquisition to older age groups and increasing the risk of severe varicella in adults. This risk can be further potentiated by the presence of large numbers of susceptible unvaccinated adult immigrants. Immigrants born in tropical countries constitute a substantial and increasing proportion of the population in Canada and in other cold high-income countries, and could benefit from varicella vaccination. There are no population-based data on the epidemiology of varicella in the immigrant compared with the non-immigrant population nor are there data on the impact of the childhood vaccination programme. Data from our study could provide insights on which subgroups of immigrants would benefit most from targeted vaccination programmes.

Added value of this study

We present results from a large population-based study of all medically attended varicella cases over an 18-year period (1996–2014) and three vaccination periods that ascertained immigrant status accurately through linkage with the provincial immigrant database. Our findings showed that immigrants from tropical countries have an increased health disparity because of varicella compared with non-immigrants, which increased after introduction of a childhood vaccination programme. Immigrants were older at varicella diagnosis and had higher age-standardised rates of varicella over the study period than did non-immigrants. More than half of all immigrant cases occurred within 2 years of arrival to Canada. Although varicella incidence decreased in both non-immigrants and immigrants after introduction of public vaccination the varicella burden shifted disproportionately to older immigrants. Certain subgroups of immigrants including women of childbearing age, young adults from Latin America and the Caribbean or south Asia, and refugees were at the highest risk.

Implications of all the available evidence

Our findings emphasise the need to provide targeted varicella vaccination programmes for immigrants younger than 50 years of age from tropical regions as soon as possible after arrival. These study findings are applicable to cold or temperate high-income countries with and without a childhood vaccination programme who are receiving large number of immigrants from temperate or tropical climates.

Immigrants make up a substantial and growing proportion of the population in Canada (23% in 2016) and other cold or temperate high-income countries.9, 10 The majority of the 250 000 new immigrants who have arrived in Canada annually in the past decade are young adults between the ages of 25 and 44 years, born in tropical countries.9 Similarly, 29% of the population in Australia, 17% in Germany, 14% in the UK, and 14% in the USA, are immigrants, many of whom were born in tropical countries.10 In these settings, immigrants are at increased risk of developing varicella compared with host populations, as shown by varicella outbreaks in young immigrant adults after arrival, with new infections occurring in 25–44% of young immigrants.11, 12, 13 Additionally, disease symptoms are more severe among immigrants, who have increased varicella-associated admissions to hospital and deaths compared with the host populations.14, 15 This risk of infection is ongoing, with reported varicella outbreaks in crowded refugee camps among the large number of refugees who arrived in Europe in 2015 and 2016.16, 17

Childhood varicella vaccination programmes result in substantially decreased varicella incidence, admissions to hospital, and deaths in all age groups because of herd immunity, and are cost-effective from a societal perspective.7 A one-dose vaccination programme resulted in a 74% decrease and a two-dose programme resulted in a 90% decrease in disease incidence in several countries.7 One key reason for the non-universal adoption of varicella vaccination is the fear of shifting varicella cases to older individuals, in whom the disease is more severe. This risk may be further potentiated by the presence of large numbers of susceptible unvaccinated adult immigrants. Varicella vaccine became available in Quebec, Canada in 1999 and a one-dose public childhood vaccination programme, given at age 12 months, was introduced in 2006.18 Vaccination coverage in 2006 was 26%, reflecting private vaccine coverage, and increased to 89% by 2008.18 A two-dose schedule was introduced in 2016, but occurred after the observation period of the present study. There are no population-based data on the epidemiology of varicella in the immigrant compared with the non-immigrant population, nor are there data on the effect of a childhood varicella vaccination programme on immigrants. We aimed to fill this knowledge gap and describe the pattern of varicella over an 18-year period before and after vaccine introduction. These data could provide insights on which subgroups of immigrants would benefit most from targeted vaccination programmes.

Section snippets

Study design and participants

We did a population-based, retrospective cohort study of all medically attended cases of varicella in Quebec, Canada from 1996 to 2014. The study base included all Quebec residents registered in the universal health-care system (Régie de l'assurance maladie du Québec; RAMQ), which includes 98% of the Quebec born and landed immigrant population living in Quebec.

The varicella cohort was created by including all medically attended varicella cases identified by varicella diagnostic codes in the

Results

A total of 231 339 varicella cases diagnosed between Jan 1, 1996, and Dec 31, 2014, were linked to 1 115 696 immigrants who arrived between Jan 1 1980, and Dec 31, 2014. 1444 cases with co-occuring herpes zoster codes were excluded. An additional 1276 immigrants from Australia, western Europe, New Zealand, and the USA were excluded. 228 619 cases of medically attended varicella occurred in the province of Quebec during the study period, resulting in 13 315 (5·8%) cases occurring in immigrants

Discussion

In this study, immigrants had a greater health disparity from varicella than did non-immigrants. Age-standardised rates were higher among immigrants younger than 50 years from all regions of origin and immigrants were older at varicella diagnosis than were non-immigrants throughout the study period. Although varicella incidence decreased substantially in all groups after introduction of the childhood vaccination programme because of herd immunity, the risk of varicella shifted disproportionally

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