Quantitative retrospective strand
A total of 247 records were identified for malaria patient who returned from abroad between January 2014 and December 2016. The median age of the patients was 33.0 years (IQR 28.0–39.5 years) and the majority was male (92%). Patients predominantly self-identified as forest goers and specialized workers (130; 53%), while the remainder identified as farmers (20; 8%), technical and service workers (20; 8%) and travelers (2; 1%). The occupation of 75 (30%) patients was unknown.
The majority of participants returned from African countries (n = 207; 84%) with the remainder traveling from Southeast Asian countries (n = 40; 16%; Fig. 2). The median time abroad was 13.5 months (IQR 6.0–331.5 months) for the 164 patients with data on duration of stay available. Patients stayed significantly longer in African countries (median 18.0 months; IQR 7.5–36.0 months) than in Southeast Asian countries (median 6.0 months; IQR 4.0–10.0 months; Mann–Whitney U = 2888, n1 = 135, n2 = 29, p < 0.0001 two-tailed, p̂a>b = 0.738). Of all participants, 108 (44%) patients had a history of acquiring malaria abroad additionally to the current infection. The proportion of patients with a previous event was significantly lower among those who had returned from the African continent (82; 40%) than those who had returned from Southeast Asia (26; 65%), although small effect size (ES) indicated low practical significance (χ2 (1; 247) = 8.78, p = 0.003, ES Φ = 0.19).
Quantitative prospective strand
Travel histories, blood samples and clinical data were collected and analyzed. Excluding two participants, 38 participants were enrolled in the study, with a median age of 36 years (IQR 30.5–42 years). All participants invited to participate in the study accepted. No one refused to participate in the study.
Of those enrolled, 87% (n = 33) were males and 79% (n = 30) reported having malaria at least once before, with 18% (n = 7) self-reporting more than 10 previous malaria infections. Of the enrolled patients, 78% were admitted after returning from African countries and 22% from Southeast Asian countries. Angola (n = 16; 42%) and Cameroon (n = 8; 21%) were the most common countries in which participants stayed during their last trip (Fig. 3).
Patients reported visits to urban (n = 25; 66%), mountainous (n = 15; 39%), rural (n = 5; 13%) and coastal (n = 4; 11%) locations, with 39% (n = 15) of patients staying exclusively at urban sites, 18% (n = 7) only at mountain sites, 13% (n = 5) visiting both urban and mountain sites, and 8% (n = 3) staying only at rural sites. Patients who traveled to Southeast Asia did not stay at urban sites (Fig. 4). Work or business (n = 31; 82%) was the most common reason for travel; other reported reasons included leisure/holiday (n = 2; 5%) and study (n = 1; 3%).
Of study participants, 58% (n = 22), 32% (n = 12), and 11% (n = 4) reported using bed nets always, frequently or not using bed nets during the latest trip, respectively. Of the 66% (n = 25) of patients who reported acquiring malaria infection during their latest trip abroad, only 8% (n = 2) reported no net use, while 60% (n = 15) used nets always and 32% (n = 8) used nets frequently.
Qualitative arm of prospective strand
The median age for IDI participants was 37 years (IQR 32.5–41.5 years). The majority of participants (n = 15) were male (11; 73%). Most participants traveled from malaria-free regions in Northern Vietnam to Cameroon (5; 33%), Angola (4; 27%) and Cambodia (3; 20%) for employment (Fig. 5). Of 15 IDIs, 9 were employees and 6 were self-employed. Reported occupations included logging (n = 9; 60%), trading (n = 4; 27%), mining (n = 1; 7%), and technical work (n = 1; 7%). Multiple responses for occupation abroad were possible. One of the participants commented the following about his occupation: “I cooperated with a Cambodian mine owner […] to mine on his property. They provided us the land, I bought timber to build houses (wooden frames, ceilings and walls).” (NAVY 313).
Quantitative retrospective strand
Plasmodium falciparum comprised 192 (78%) malaria cases. Of these, 181 (94%) were diagnosed in patients who returned from Africa. While P. falciparum infection prevailed in travelers who returned from Africa (87% of all malaria cases acquired in Africa), infection with P. vivax was predominant in patients who returned from Southeast Asian countries (60% of all malaria cases acquired in Southeast Asia; Fig. 6). None of the patients who returned from Southeast Asian countries presented with P. malariae or P. ovale, while four infections with P. malariae or P. ovale (two each representing 1%, each, of all cases) were diagnosed in patients who returned from African countries.
Among 173 patients with information on duration to parasite clearance, 51 (30%) patients, including 41 (30%) patients with P. falciparum infection, still had measurable parasitemia by microscopy on day 3. The proportion of patients with previous history of infection was significantly lower among patients whose parasitemia cleared within 3 days or less (42%) than among patients with detectable parasitemia on day 3 (63%), although small effect size indicated weak association between time to parasite clearance and history of previous malaria infection (χ2 (1; 173) = 6.32, p = 0.012, ES Φ = 0.19). The difference in proportions of all cases with detectable parasitemia on day 3 was not significant between patients returned from the African continent and patients returned from the Southeast Asian region (χ2 (1; 173) = 0.29, p = 0.589, ES Φ = 0.04). The difference in proportions of P. falciparum cases with detectable parasitemia on day 3 was also not significant between patients who returned from the African continent and patients who returned from the Southeast Asian region (χ2 (1; 138) = 1.42, p = 0.234, ES Φ = 0.10).
Quantitative prospective strand
All patients experienced characteristic fever patterns and other malaria symptoms prior to admission and presented with a number of malaria symptoms, including fever (median temperature 38.0 °C, IQR 37.0–39.0 °C) and rapid pulse (median 85.5 beats/min, IQR 80.0–93.8 beats/min). Common malaria symptoms registered upon admission are listed in Table 1. Median duration between return from abroad and onset of symptoms was 9 days (IQR 2.5–14 days); the median duration between the onset of symptoms and admission to the hospital was 3 days (IQR 2–7 days).
All patients (38; 100%) tested positive for malaria by microscopy and/or RDT and/or PCR. Of these malaria patients, 68% (n = 26) were diagnosed with P. falciparum, 16% (n = 6) with P. vivax, 8% (n = 3) with P. ovale, 5% (n = 2) with P. malariae and 3% (n = 1) had a discrepant result of P. malariae by PCR and P. ovale by microscopy (Fig. 7). Microscopy, RDT, and PCR were not significantly different in sensitivity (Cochran’s Q = 5.56, p = 0.062). In respect to specificity, all three methods detected P. falciparum in 24 (63%) patients and P. vivax in 5 (13%) patients. RDT did not detect any of the P. malariae and P. ovale cases, and one of six cases (17%) of P. vivax, but detected two (8%) cases of P. falciparum, one of which was not detected by microscopy and another by both microscopy and PCR.
Twenty-five (96%) P. falciparum cases and all three P. ovale cases originated in the African continent, while six (100%) of P. vivax infections were imported from the Southeast Asian region; two cases of P. malariae infection (as diagnosed by PCR) were imported from Africa and one from the Southeast Asia (Fig. 8). Day 3 parasite clearance rates were 58% (n = 15) and 50% (n = 3) for P. falciparum and P. vivax, respectively. The proportions of patients with previous history of infection were not significantly different between groups with parasite clearance within 3 days or less (87%) and with detectable parasitemia on day 3 (64%) (p = 0.215; Fisher’s exact test). There was a very weak correlation between d0 parasite density and the number of days to parasite clearance for P. falciparum (Sperman’s correlation analysis: rs = − 0.027, p = 0.900) and for P. vivax (Sperman’s correlation analysis: rs = − 0.348, p = 0.497). For P. falciparum, the association between the time to parasite clearance and the time from symptoms onset to hospital admission was also weak (Sperman’s correlation analysis: rs = 0.085, p = 0.700).
Qualitative arm of prospective strand
Upon return to Vietnam, six participants (40%) were diagnosed with P. falciparum, four (27%) were diagnosed with P. vivax, and one (7%) was diagnosed with P. ovale. Diagnosis for four participants (27%) was not recorded. In patients who returned from the African continent, P. falciparum comprised 42% of malaria cases. P. vivax was imported from Southeast Asian countries only, while a single P. ovale case arrived from the African continent.
Qualitative arm of prospective strand: knowledge of malaria
Perceived susceptibility IDI questions related to perceived susceptibility covered general knowledge of malaria before participants travel abroad and knowledge of the causes of malaria, specifically. Before traveling to their foreign work site, 67% (n = 10) reported having some prior knowledge of malaria, while 33% (n = 5) reported having no previous knowledge. Of 10 participants with prior knowledge, 40% (n = 4) learned about malaria on the internet while conducting research about the country they were preparing to visit, 60% (n = 6) learned from friends or acquaintances who had traveled to endemic countries, and only one participant reported being informed about malaria by a future employer. Participants who were unaware of malaria before the trip learned about malaria while in the country of their destination from co-workers (n = 1; 20%), when co-workers became sick (n = 2; 40%) or when the participant became sick (n = 1; 20%). Some discussed the challenges in finding information on malaria before departure: “Before going to Angola, I self-searched about Angola on the internet […] no information about epidemics. I only knew about malaria after I got it in Angola.” (NAVY 306).
Ten participants who had previous knowledge of malaria reported knowing that malaria is transmitted by mosquito bites (n = 3; 30%), that nets (n = 3; 30%) and protective clothing (n = 1; 10%) reduce risk from mosquitoes biting and that forest goers can get malaria (n = 1; 10%). Additional responses included awareness of malaria drugs (n = 2; 20%) and malaria vaccines (n = 1; 10%). Of those who reported knowledge of malaria prior to their trip, four participants (40%) reported incorrect knowledge, including not getting malaria in Vietnam “because I eat very spicy food”; malaria is caused by “chemicals directly discharged in the environment”; that “West Africa has no malaria”; and that exposure to contaminated water presents a risk for acquiring malaria (n = 2; 20%). Participants could provide more than one response regarding their knowledge of malaria.
Cues to action were covered in the IDI with the inclusion of questions on media sources accessed while abroad. Of all participants, 33% (n = 5) did not access any media. Most media accessed were Vietnamese websites, television or Facebook, due to language barriers to accessing local media (n = 7; 47%). Only 27% of participants (n = 4) reported watching local television or websites. Only one participant who accessed Vietnamese websites reported learning about malaria outbreaks from the Vietnamese community, while all four participants who watched local television received warnings about malaria and other disease outbreaks. Of all participants, 20% (n = 3) reported seeking treatment, both abroad and in Vietnam, upon advice from colleagues.
Qualitative arm of prospective strand: transformation of knowledge about malaria
Change in knowledge about malaria was covered by questions about the cause of patient’s most recent malaria infection and malaria symptoms. With regard to the causes of patient’s malaria, the majority of participants (n = 12; 80%) were aware that their malaria was caused by mosquito bites. Of all participants, eight (53%) erroneously believed that contaminated water sources were also a cause of malaria due to presence of viruses, bacteria or chemical contamination. Participants were able to report multiple answers to this question.
Based on their own or a co-worker’s experience, all participants were able to accurately describe malaria symptoms. Among seven most commonly reported symptoms were fever or severe fever (n = 14; 93%), chills (n = 9; 60%), fatigue (n = 3; 20%), headache (n = 3; 20%), and muscle pain (n = 3; 20%) (Table 2): “On 18 Feb, I got tired, [had] fever, headache, dizziness, but not chills. […] Brothers said I got malaria when I had symptoms of backache, diarrhea and headache.” (NAVY 315).
Perceived severity All participants considered symptoms severe enough to warrant their visit to health facility or contact of a private provider, both abroad and in Vietnam. The top three reasons for reporting to the hospital upon malaria symptoms onset were: malaria can be deadly (n = 6; 40%), the symptoms participants experienced were life-threatening (n = 11; 73%), and malaria or experienced symptoms could cause permanent damage (n = 4; 27%). The median duration between symptoms onset and reporting to the hospital was 5 days (IQR 4.0–9.5 days), and did not differ significantly between patients with prior knowledge of malaria (median 5.0 days, IQR 4.0–8.0 days) and without prior knowledge (median 6.5 days, IQR 2.5–10.5 days) (Mann–Whitney U = 15, p = 0.933).
Qualitative arm of prospective strand: treatment seeking behavior
Perceived Barriers to Treatment Abroad Of patients participating in the IDIs, 12 (80%) developed malaria symptoms at their foreign work site one or more times. All 12 participants went to the hospital, a district health center or a private doctor; of the 12, two (17%) participants called a private doctor prior to hospital admission, one participant self-treated with over-the-counter medicine, and one first attempted to treat cold symptoms. None of the participants reported barriers that would prevent them from seeking health care in a foreign country. A typical response was: “There was no difficult[y]. Health center was empty, didn’t have to line up because it was in district level. When I stayed in Angola from 2012 to 2016, my shop [was] near a provincial hospital. I was friend with some Vietnamese specialists. They said Cuban, North Korean, Russian specialists were better. Vietnamese specialist often worked in anesthesia and surgery.” (NAVY 15). Of all participants, 33% (n = 4) who worked for a company abroad reported that the company paid for their medical treatment and provided an interpreter and transportation to the doctor’s office. Participants acknowledged the availability of anti-malarial drugs and RDTs at pharmacies in the countries they visited (n = 5; 42%), easy access to Vietnamese specialists (n = 4; 33%), and easy access to private and public hospitals (n = 3; 25%). Only one self-employed patient noted that treatment and medication were expensive, and two participants (17%) said that language barrier was an obstacle in communicating with a doctor. Some participants provided multiple answers. These experiences were found in the qualitative interviews, where a typical discussion was: “In Cameroon, I was treated in a private hospital of indigenous people. I did not have to queue, I had a little difficulty in communication.” (NAVY 312).
Perceived Barriers to Treatment in Vietnam All participants sought health care upon malaria symptoms onset in Vietnam. Of all participants, 47% (n = 7) reported going directly to the NHTD or the NIMPE clinic based on results of an internet search (n = 4; 27%) or co-worker recommendation (n = 2; 13%); 33% (n = 5) went to a district hospital, followed by transfer to the NHTD or the NIMPE clinic based on hospital (n = 3; 20%) or co-worker (n = 2; 13%) recommendations; and 20% (n = 3) reported going to a private doctor with subsequent transfer to one or two district hospitals and then the NIMPE clinic (n = 2; 13% based on hospital recommendations and n = 1; 7% based on co-worker recommendation) (Table 3). Representative comments about treatment in Vietnam were: “I have only been treated in Vietnam. Advantages: Enthusiasm [of] doctors, full of medicines. Difficulties: Hospital at district level in Hanoi couldn’t diagnose the exact disease. […] I was introduced to NHTD by brothers working in Cameroon.” (NAVY 17).
Qualitative arm of prospective strand: use of protective measures
Five (33%) participants reported having no knowledge of malaria prior to traveling abroad; two of them reported not having any protective measures upon arrival. Hiring companies provided protective measures for six (40%) participants and another six (40%) participants brought protective measures (hammock nets and repellents) with them. One participant was provided with a net by a friend. Protective measures provided by the companies included bed nets (n = 4), treated nets (n = 2), repellent (n = 2), air-conditioned and/or screened areas for work and lodging (n = 4). A participant in the qualitative arm explained how he prepared himself before departure: “When I started a business in Africa, I prepared myself, including insect repellent spray and the type I buy in Vietnam. Quinine malaria drug I was given by a Korean [business] partner.” (NAVY 314).
Perceived Benefits When asked about preventive measures they knew, three (20%) respondents said that “malaria cannot be prevented”; 11 (73%) named bed nets or hammock nets; five (33%) named repellent; and three (20%) mentioned the use of air-conditioning. Other responses included “clean eating”, “clean water” and “clean room” (n = 6; 40%), as well as use of anti-insect screens, mosquito traps, avoiding mosquito bites at certain times of the day and wearing long-sleeved clothes.
Of all respondents, six (40%) reported that they were not aware of treated nets. Of the six respondents who knew about treated nets, one respondent said the treated net was better than untreated, two respondents said it did not help as it was used only at night or inside where there were no mosquitoes, and three respondents reported never having used treated nets.
When asked about protective measures used, 10 (67%) participants reported using bed nets; four (27%) participants reported using repellents, two (13%) reported the use of medication, two (13%) reported staying in air-conditioned room, and two (13%) participants reported using hammocks. Two participants (13%) reported using no protective measures at all, with one stating that malaria is unavoidable (Fig. 9). Participants could provide more than one response regarding their use of protective measures. This statement, from an IDI with malaria patients, was typical: “In my neighborhood, there are many mosquitoes, big mosquitoes, and I usually slept with net at night.” (NAVY 315).
Of 10 respondents who reported frequency of preventive measures use, 50% (n = 5) always and 20% (n = 2) frequently used bed nets or hammock nets, only one participant reported frequent use of repellent (Table 4).
Qualitative arm of prospective strand: future travel plans
Only 20% (n = 3) participants indicated no intention of returning abroad, citing danger of malaria, devaluation of currency, criminal situation in a foreign country and poor health. All three of these participants traveled abroad only once, with duration of trips between 1 and 28 months. One participant who spent 17 years in Angola was not sure if he would return to Angola. The remaining 73% (n = 11) planned to return abroad soon after treatment. Of them, 64% (n = 7) have traveled abroad two or more times and have spent a total of 30 or more months abroad, while only 27% (n = 3) have traveled once for a duration of 7–12 months (Fig. 10).