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Abstract

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

Background. Visiting friends and relatives (VFRs), especially young VFRs, are increasingly recognized in the industrialized world as a high-risk group of travelers.

Methods. We performed a descriptive, cross-sectional design study of cases of malaria, hepatitis A, and typhoid reported to the Quebec registry of notifiable diseases between January 2004 and December 2007, occurring in VFRs and non-VFRs travelers.

Results. VFRs account for 52.9% of malaria cases, 56.9% of hepatitis A cases, and 94.4% of typhoid cases reported in Quebec travelers. Almost all (91.6%) of the malaria cases among VFRs were acquired in Africa, particularly in sub-Saharan Africa. An important proportion of malaria cases among VFRs (86.4%) were due to Plasmodium falciparum. The vast majority (76.6%) of typhoid fever cases among VFRs were reported by travelers who had visited the Indian subcontinent. Among VFRs, 40% of total cases were under 20 y of age, compared to less than 6% among non-VFRs. Those under 20 years of age also accounted for 16.9% of malaria cases, 50% of typhoid cases, and 65.2% of hepatitis A cases among VFRs.

Conclusion. Our study clearly shows that VFR children should be a primary target group for pre-travel preventive measures.

Quebec is Canada's second most populous province with almost 8 million inhabitants,1 for the most part French-speaking (79%), and with a different immigration profile from the rest of Canada.2,3 In 2008, the regions of origin of Canadian immigrants were mainly China (11.9%), the Philippines (9.6%), and India (9.9%), whereas in Quebec, more than 30% of immigrants came from Africa, including North Africa and sub-Saharan Africa.3 Recent Quebec immigrants are generally young, with nearly 30% under the age of 25. In the 2006 census, immigrants accounted for 11.5% of Quebec's population.4 Immigrants who return to their country of birth to visit friends and family are referred to as visiting friends and relatives (VFRs). The number of trips taken by Quebec VFRs reached 208,000 in 2008, an increase of at least 50% since 2000. Between 2004 and 2007, VFRs accounted for 10.0 to 14.5% of trips taken by Quebec residents outside Canada and the United States.5

VFRs are recognized in Canada and in other industrialized countries as a group of at-risk travelers,6–8 being less likely to seek a pre-travel consultation. The related costs as well as an underestimation of the risks and a false sense of natural immunity, may contribute to such behaviors.6 Access to travel health services may also be limited by cultural and linguistic barriers and lack of awareness about such services. VFRs make more last-minute trips, often with children and travel for longer periods; 43% are away for more than 3 weeks, compared to 15% of tourists.5 They may also visit rural areas more often and frequently stay with local people. They are at higher risk of consuming contaminated food and beverages, and of exposure to respiratory and vector-borne diseases. The frequency of malaria, typhoid fever, tuberculosis, hepatitis A and B, and other vaccine-preventable diseases is higher in VFRs than in other types of travelers.7–14

The situation is even more worrisome among children of immigrant parents. According to Canadian data from 2008, 11% of VFRs are under 20 y of age.5 The risk of contracting malaria and developing complications is especially high in this age group.15–17 Furthermore, typhoid fever is a serious illness that is usually acquired abroad, and young people between the ages of 5 and 19 are most at risk.18

This article describes certain characteristics observed in cases of malaria, hepatitis A, and typhoid fever reported among VFRs living in Quebec compared to cases reported among other types of Quebec travelers from 2004 to 2007. Changes over time in the proportion of cases among VFRs are presented. Recommendations are made based on these results to provide the best possible care to VFRs, and especially to VFR children.

Methods

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

Study Population

This study includes all the cases of malaria, hepatitis A, and typhoid fever reported in the provincial reportable disease database between January 2004 and December 2007. A traveler was defined as a resident of Quebec who traveled outside of Canada, the United States, and Europe. VFRs were defined as immigrants and their offsprings who are ethnically and/or racially distinct from the majority of the population of their country of residence, and who return to their country of origin to visit family or friends.10 They typically travel from a developed country to a less developed country. Our study includes immigrants, their spouse or children born in the host country, and also overseas adoptees returning to visit their country of origin after their arrival in Quebec. The “non-VFRs” category includes those who traveled for tourism, work, study, or volunteering.

Data Sources

The provincial reportable disease information system contains, for each reported case, information such as date of birth, gender, reporting date, country of acquisition, and clinical course. Each reported case generally undergoes an epidemiological investigation by the public health department of the person's region of residence. This investigation also provides, when appropriate, information on risk factors for acquiring the infection such as the destination, length, and purpose of the trip. For the purposes of this study, a denominalized copy of this investigation was requested for each eligible case. A pretested form was used to extract pertinent data.

The number of Quebec travelers is not available directly so we relied on estimation for the number of trips by Statistics Canada which comes from surveys and counts of travelers conducted at border crossings.5

Data Analysis

This study uses a cross-sectional design. The proportion of cases by purpose of trip is listed, followed by sociodemographic characteristics and risk factors. The proportions of cases among VFRs are compared to other Quebec data collected between 1997 and 2002.7,19

The chi-square test is used to compare VFRs and non-VFRs as to the distribution of cases by age group (three categories), gender, trip length (three categories), and travel health consultation before departure.

The project was approved by the administrative and research ethics board of Charles-LeMoyne Hospital, Longueuil, Canada.

Results

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

Description of the Study Population

A total of 772 files were eligible for the study throughout the province, including 318 cases of malaria, 398 cases of hepatitis A, and 56 cases of typhoid fever. We obtained 727 files (93.5%) from public health departments, of which 657 (81.5%) had undergone an epidemiological investigation and 363 (49.9%) were travelers. The purpose of the trip was known for 309 cases in travelers, with 183 VFRs.

Among the 126 non-VFRs, the purpose of the trip was either tourism (N = 70), or study, work, or volunteering (N = 56).

Description of Cases Among VFRs and Non-VFRs

The description of the proportion of cases among travelers by purpose of trip and disease is shown in Table 1. Statistics Canada data on all trips taken by Quebecers during the period of study is included to better assess the number of cases among VFRs.5 Comparisons of certain characteristics between VFRs and non-VFRs are shown in Table 2.

Table 1.  Distribution of cases by purpose of trip and disease among travelers, Quebec, 2004 to 2007 (N = 309)
Purpose of tripMalaria (n = 157)Hepatitis A (n = 116)Typhoid fever (n = 36)Proportion of trips taken by all Quebecers, 2004 to 2007 (n = 5,435,000)
  1. VFR = visiting friends and relatives.

Tourism12.7%42.2%2.8%76.0%
Work, study, and volunteering34.4%0.9%2.8%10.1%
VFR52.9%56.9%94.4%13.9%
Table 2.  Description of cases among VFRs and non-VFRs by gender, age, trip length and pre-travel consultation for all of the diseases under study, Quebec, 2004 to 2007 (N = 309)
 MalariaTyphoid feverHepatitis ATotal
VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)
  1. VFR = visiting friends and relatives.

Total83743426650183126
Gender(N = 83)(N = 74)(N = 34 )(N = 2)(N = 66)(N = 50)(N = 183)(N = 126)
 Male57 (68.7)56 (75.7)17 (50.0)2 (100.0)37 (56.1)25 (50.0)111 (60.7)83 (65.9)
 Female26 (31.3)18 (24.3)17 (50.0)0 (0.0)29 (43.9)25 (50.0)72 (39.3)43 (34.1)
Age (y)(N = 83)(N = 74)(N = 34)(N = 2)(N = 66)(N = 50)(N = 183)(N = 126)
 <2014 (16.9)3 (4.1)17 (50.0)0 (0.0)43 (65.2)4 (8.0)74 (40.4)7 (5.6)
 20–5462 (74.7)61 (82.4)16 (47.1)2 (100.0)22 (33.3)40 (80.0)100 (54.7)103 (81.7)
 ≥557 (8.4)10 (13.5)1 (2.9)0 (0.0)1 (1.5)6 (12.0)9 (4.9)16 (12.7)
Length of travel (d)(N = 81)(N = 66)(N = 33)(N = 1)(N = 64)(N = 47)(N = 178)(N = 114)
 ≤147 (8.6)13 (19.7)0 (0.0)0 (0.0)1 (1.6)29 (61.7)8 (4.5)42 (36.8)
 15–2924 (29.6)5 (7.6)7 (21.2)0 (0.0)9 (14.1)8 (17.0)40 (22.5)13 (11.4)
 ≥3050 (61.8)48 (72.7)26 (78.8)1 (100.0)54 (84.3)10 (21.3)130 (73.0)59 (51.8)
Pre-travel consultation(N = 9)(N = 29)(N = 5)(N = 1)(N = 24)(N = 19)(N = 38)(N = 49)
 Yes6 (66.7)18 (62.1)1 (20.0)1 (100.0)5 (20.8)1 (5.3)12 (31.6)20 (40.8)
 No3 (33.3)11 (37.9)4 (80.0)0 (0.0)19 (79.2)18 (94.7)26 (68.4)29 (59.2)

VFRs represent the largest category of travelers for each of the three diseases. Among VFRs, 40% of cases were under 20 years of age, compared to less than 6% among non-VFRs (p < 0.000). In Canada, only 11% of VFRs were under 20 years of age in 2008,5 but in our study, this age group accounted for 16.9% of malaria cases, 50% of typhoid cases, and 65.2% of hepatitis A cases among VFRs. The median age of cases among VFRs is 32 years for malaria (vs 37.5 y among non-VFRs), 19.5 years for typhoid fever (vs 34.5 y), and 15.5 years for hepatitis A (vs 37 y).

As for trip duration, 73% of cases among VFRs had traveled for 30 days or more, compared to 51.8% of non-VFRs (p < 0.000). No case among VFRs was reported with a trip of 1 week or less. However, it is worrisome to note that a fair proportion of cases among VFRs occurred following a trip of intermediate length, ie, from 15 to 29 days, which is almost 30% of the malaria cases and 21.2% of the typhoid cases. The proportion of hepatitis A cases reported following a trip of 14 days or less is clearly higher among non-VFRs (61.7%) compared to VFRs (1.6%).

The highest proportion of cases among VFRs occurred in the 3rd quarter, between July 1 and September 30: 31.3% of malaria cases, 41.2% of typhoid cases, and 56.1% of hepatitis A cases (Table 3). This seasonal variation in cases among VFRs differs significantly (p = 0.004) from non-VFRs.

Table 3.  Distribution of cases by disease and date of episode among VFRs and non-VFRs, Quebec, 2004 to 2007 (N = 309)
 MalariaTyphoid feverHepatitis ATotal
VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)
  1. VFR = visiting friends and relatives.

Total83743426650183126
January 1 to March 3115 (18.1)15 (20.3)5 (14.7)0 (0.0)13 (19.7)18 (36.0)33 (18.0)33 (26.2)
April 1 to June 3014 (16.9)16 (21.6)12 (35.3)0 (0.0)8 (12.1)19 (38.0)34 (18.6)35 (27.8)
July 1 to September 3026 (31.3)21 (28.4)14 (41.2)1 (50.0)37 (56.1)7 (14.0)77 (42.1)29 (23.0)
October 1 to December 3128 (33.7)22 (29.7)3 (8.8)1 (50.0)8 (12.1)6 (12.0)39 (21.3)29 (23.0)

In terms of gender, no statistically significant difference was found between VFR and non-VFR cases. Pre-travel consultation data is to be interpreted with care due to lack of information in most cases (222/309), and even when it is available, we cannot rule out social desirability bias in the answer.

Description of Cases by Trip Destination

Table 4 shows the main regions of acquisition reported for the three diseases under study, for VFRs and non-VFRs.

Table 4.  Distribution of cases by disease and main acquisition regions reported among VFRs and non-VFRs, Quebec, 2004 to 2007 (N = 309)
 MalariaTyphoidHepatitis ATotal
VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)VFR N (%)Non-VFR N (%)
  1. VFR = visiting friends and relatives.

Total83743426650183126
Sub-Saharan Africa62 (74.7)51 (68.9)1 (2.9)0 (0.0)6 (9.1)1 (2.0)69 (37.7)52 (41.4)
North Africa0 (0.0)0 (0.0)0 (0.0)0 (0.0)21 (31.9)1 (2.0)21 (11.5)1 (0.7)
Africa unspecified14 (16.9)9 (12.2)0 (0.0)0 (0.0)0 (0.0)0 (0.0)14 (7.7)9 (7.1)
Latin America (except Cuba, Mexico)0 (0.0)7 (9.4)0 (0.0)1 (50.0)8 (12.1)8 (16.0)8 (4.4)16 (12.7)
Cuba, Mexico, Dominican Republic0 (0.0)3 (4.0)1 (2.9)0 (0.0)6 (9.1)30 (60.0)7 (3.8)33 (26.2)
Haiti5 (6.0)2 (2.7)3 (8.8)0 (0.0)1 (1.5)2 (4.0)9 (4.9)4 (3.2)
Indian subcontinent2 (2.4)0 (0.0)26 (76.6)0 (0.0)14 (21.2)0 (0.0)42 (22.9)0 (0.0)
Asia (except Indian subcontinent)0 (0.0)1 (1.4)1 (2.9)0 (0.0)3 (4.5)2 (4.0)4 (2.2)3 (2.4)
Middle East0 (0.0)0 (0.0)2 (5.9)0 (0.0)5 (7.6)1 (2.0)7 (3.8)1 (0.7)
Others or unknown0 (0.0)1 (1.4)0 (0.0)1 (50.0)2 (3.0)5 (10.0)2 (1.1)7 (5.6)

Among VFRs, 79.8% of cases traveled to Africa or the Indian subcontinent, compared to 49.2% of cases among non-VFRs.

Virtually all (91.6%) of the malaria cases among VFRs were acquired in Africa, particularly in sub-Saharan Africa. The Plasmodium falciparum type accounts for 86.4% of malaria cases among VFRs. The vast majority (76.6%) of typhoid fever cases among VFRs were reported by travelers who had visited the Indian subcontinent. For hepatitis A, over 60% of cases among VFRs were acquired in Africa (including 31.9% in North Africa) or the Indian subcontinent. For non-VFRs, 60% of cases contracted hepatitis A while visiting so-called sunshine destinations favored by Quebecers, namely Cuba, Mexico, and the Dominican Republic.

Changes in the Burden Among VFR Travelers

Data were compared with Provost et al.7 and De Serres et al.19 studies. Since 2000 to 2002, the proportion of malaria cases attributed to VFRs more than doubled (52.9% vs 25%), and for typhoid, it increased to 94.4% from 86%.7 For hepatitis A, the proportion of cases related to VFRs was 30% between 1997 and 1999, while the results of our study show a proportion of 56.9%.19 Unfortunately, we do not have age-specific data for those two studies, which would help determine if some age groups are now more affected than others.

Discussion

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

VFRs: High-Risk Travelers

We note that VFRs are a group of travelers disproportionately affected by the diseases under study. The general upward trend of immigration cannot by itself explain the increase in the proportion of cases observed among VFRs, since the percentage of trips taken by VFRs is stable.5 We do not have data on the main destinations favored by Quebec VFRs. However, in recent years, Quebec has become home to a growing number of immigrants from sub-Saharan Africa.4 It has also seen immigration from Haiti, which accounts for 6.7% of all immigrants in 2006.20 This migration profile from high-risk areas may explain in part the increase in the proportion of cases observed in VFRs. Interestingly, we note that the proportion of malaria cases due to P falciparum is slightly higher in Quebec (72.3% overall and 86.4% among VFRs) than in the United States (63%).21 This may be because the rest of North America's immigration profile is from areas less at risk for P falciparum. Another reason for the increase in the proportion of cases seen in VFRs could be a decrease among other travelers due to better awareness of preventive travel services.

Lastly, VFRs from Quebec present the same risk factors as other VFRs.6–14 As shown in our study, they travel for long periods and are less likely to opt for a pre-travel consultation.

High Proportion of Cases in Those Under Age 20

There is a significant difference in the proportion of cases among young VFRs and young non-VFRs. Although parents may have a partial immunity against diseases such as malaria or typhoid that are endemic in their country of origin, their children born in Quebec do not benefit from the same natural protection. It would have been interesting to see the proportion of hepatitis A cases among VFRs born in Quebec vs VFRs born outside Quebec, but this information was not available.

The tendency of VFRs to travel with their children during the summer holidays may explain the high proportion of cases among children. The custom of presenting a newborn child to the extended family also means that very young children are traveling to at-risk areas.

Solutions

Quebec VFRs have been recognized as high-risk travelers since the Provost et al. study.7 Preventive care provided to Quebec travelers seems to be paying off, considering the significant increase in the number of trips compared with the relative stability in the number of cases of the diseases under study. For VFRs, however, a lot of work remains to be done, and our study clearly shows that children of VFRs should be a primary target group. A more concerted effort should be made to reach them, since despite initiatives by some travel health clinics to make pre-travel services more accessible, such as special rates for children, information meetings for immigrants, and training for family physicians working in multi-ethnic settings, VFRs continue to bear a heavy burden of the diseases under study.

Practitioners caring for immigrant patients should be made aware of the significant burden of travel-related illnesses in these communities, especially in children. They should remain up to date on recommended preventive measures for travelers, and know when to refer the more complex cases to specialized travel health clinics. For example, health professionals need to make sure that their patients' routine vaccinations are complete, and those who prescribe malaria chemoprophylaxis should receive adequate training to avoid medication errors. The increasing resistance of Salmonella typhi to antibiotics points to the need of a more effective and targeted promotion of typhoid fever vaccination among VFRs. It is worth mentioning that the benefits of prevention among VFRs extend beyond immigrant communities. For example, hepatitis A vaccination of young VFRs could help prevent outbreaks in day-care centers, which are attended by more than two-thirds of Quebec children between the ages of 6 mo and 5 y.22

At the government level, a health information package on routine vaccinations and other recommended preventive measures before a person's return trip to their country of origin should be provided to new immigrants.

Moreover, recent initiatives in Quebec's Provincial Health Insurance provisions, such as the reimbursement of anti-malarial drugs and the use of the combined hepatitis A and B vaccine in the school-based vaccination program, could lower the burden of these diseases among young VFRs in coming years.

Limits and Strengths

The data sources can bias some of our estimates. Notifiable diseases are often under-diagnosed and under-reported.23–26 Epidemiological questionnaires are not uniform between public health departments, thus resulting in missing information, particularly on the trip purpose and pre-travel consultation. Statistics Canada data estimate the number of trips, and not the number of travelers. This can result in an overestimation in the number of travelers, because one can make several trips a year. However, this may be less significant for VFRs, since they typically return to their country of origin with their children during summer holidays. Statistics show that VFRs travel back to Quebec mainly in the third quarter (33%),5 which is consistent with our results.

Our study examined all reported cases of malaria, hepatitis A, and typhoid fever among Quebec travelers between 2004 and 2007, providing a complete picture of the epidemiologic situation. Since we used a similar methodology to the one used in 2000 to 2002, one can compare changes over time and identify the groups that require more preventive work.7 Typhoid fever data should be interpreted with caution because of their small numbers, although our results are consistent with other studies.7,8,27

It would be interesting to examine the pre-travel consultation determinants among VFRs in a future study. There is evidence that likelihood of a pretravel consultation increases with time spent living in Canada.28 Empirically, we also note that second generation immigrants are more likely to consult than those born outside Quebec. Moreover, with an increasing number of mixed-race couples in Quebec society, this demographic trend would probably influence future behaviors of VFRs. A recent article proposed a more detailed description of VFRs, and included a framework for risk assessment that could be useful for the Travel Health practitioner.29

Conclusion

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

In Quebec, as in the rest of Canada and the industrialized world, VFRs, especially young VFRs, are high-risk travelers. Public health authorities should come up with strategies to better reach this vulnerable group and to provide it with effective preventive measures. Surveillance studies at regular intervals on the health of travelers are needed to document the efficacy of these interventions.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

Unrestricted funding was received from Institut national de santé publique du Québec (INSPQ).

Declaration of Interests

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References

Y.-G. Bui received speaking fees from GlaxoSmithKline and Sanofi Pasteur. The other authors state they have no conflicts of interest to declare.

References

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusion
  7. Acknowledgment
  8. Declaration of Interests
  9. References