Abstract
Background
Imported malaria poses a growing challenge to elimination efforts in non-endemic countries, with migrant workers constituting a high-risk population. Understanding care-seeking behaviours and diagnostic delays is crucial for preventing secondary transmission. This study investigated the systemic determinants of diagnostic delays among returning migrant workers.
Methods
Using data from the national surveillance system, we retrospectively analyzed a cohort of 2098 imported malaria cases involving migrant workers reported in Jiangsu Province, China, between January 2012 and December 2019. Delayed care-seeking was defined as > 3 days from symptom onset, and diagnostic delay as > 2 days post-consultation. Multivariate regression analyses were used to assess the relationships between demographic characteristics, clinical presentation, healthcare utilization patterns, socioeconomic factors (including destination city GDP), and time-to-diagnosis outcomes.
Results
Sub-Saharan Africa accounted for the largest share of infection origins (78.65%, 1650/2098), with Plasmodium falciparum being the leading species (78.41%, 1645/2098). Factors significantly associated with a decreased risk of diagnostic delay included delayed care-seeking > 3 days (OR = 0.62, 95% CI 0.44–0.88), non-severe malaria (OR = 0.57, 95% CI 0.38–0.86), symptom onset > 1 month after-entry (OR = 0.46, 95% CI 0.31–0.69), and initial consultation at municipal (OR = 0.20, 95% CI 0.11–0.37) or provincial (OR = 0.27, 95% CI 0.16–0.52) institutions. Conversely, higher destination city GDP (Second-level: OR = 2.74, 95% CI 1.88–400) were associated with increased diagnostic delays.
Conclusions
Our findings highlight the need to increase clinician awareness regarding malaria diagnosis, particularly for patients presenting early with mild symptoms. Enhancing primary healthcare diagnostic capacity and educating migrant workers about promptly seeking medical advice are critical for preventing the re-establishment of malaria.
Keywords: Imported malaria, Migrant workers, Diagnosis delay, Care-seeking behavior, Travel medicine
Background
In countries that have achieved or are approaching elimination, imported cases now constitute the majority of reported infections, posing a persistent risk of re-introduction wherever competent Anopheles vectors remain [1–4]. Historically, inadequate management of mobility-associated transmission contributed to the failure of malaria elimination programmes in the 1950 s and 1960 s [5]. In the current era of globalisation, international labour migration has magnified this risk, making imported malaria a key challenge for sustaining elimination.
China initiated the National Malaria Elimination Action Plan in 2010 and received official malaria-free certification from the World Health Organization on June 30, 2021 [6, 7]. At the same time, rapid development and globalization have increased population mobility, thereby complicating sustained elimination efforts [8, 9]. Malaria has been the most frequently reported travel-associated infectious disease in China, accounting for 27,497 cases (86.6% of all imported infectious diseases) from 2005–2016 [10, 11]. In contrast to the United States and many European countries, where imported malaria is commonly seen among people visiting friends or relatives, cases in China are mainly associated with migrant workers returning from endemic areas [12–16].
Migrant workers, while contributing to economic development in both host and home countries, encounter numerous difficulties, including hazardous occupational conditions in industries such as mining, construction, and logging, as well as issues such as discrimination and breaches of employment contracts [17, 18]. Millions of these workers, particularly those in lower-skilled positions, face substantial physical and mental health challenges, which are often exacerbated by inadequate access to healthcare [19–22]. Upon returning from malaria-endemic tropical regions, these migrant workers can introduce malaria into areas previously declared malaria-free, creating significant public health risks [23–25]. Consequently, timely detection, accurate diagnosis, and effective management of imported malaria cases among migrant populations are crucial for reducing fatalities and preventing disease resurgence.
Timely recognition and treatment of imported malaria depend largely on how soon patients seek medical attention after symptom onset and how rapidly clinicians establish the diagnosis. To date, however, little research has been conducted on the healthcare access and service needs of migrant workers [26–31]. Moreover, existing studies often address patient and doctor delays independently, leaving the association between the two among migrant workers unclear [32–37]. Therefore, this study aims to (1) describe patterns of care-seeking delay and diagnostic delay in cases of imported malaria occurring in migrant workers; (2) investigate the associations among these delays; (3) explore factors influencing diagnostic delays; and (4) propose interventions to improve early detection.
Methods
Study setting
Located in southeastern China (Fig. 1A), Jiangsu Province is economically advanced and had an estimated population of 85 million as of 2022 (National Bureau of Statistics of China, 2023; Statistics Bureau of Jiangsu Province, 2023). The region’s GDP per capita consistently ranks among the top three nationally. Although Jiangsu has reported no local malaria transmissions since 2012, the province continues to document high numbers of imported malaria cases, with annual occurrences ranging between 198 and 405 from 2012 to 2019 [32].
Fig. 1.
Location of the study area A and classification of cities by level of economic development B
Migrant workers with imported malaria
In China, a malaria case is classified as imported only if all of the following criteria are satisfied: (i) laboratory confirmation of malaria; (ii) travel to malaria-endemic areas outside China during the malaria transmission season; and (iii) symptom onset within one month of return to China during the local transmission season [38]. Cases that do not satisfy these criteria are classified as local. Case classification is determined by provincial or national experts during regular routine meetings when necessary.
For the purposes of this study, “migrant workers” refers specifically to Chinese nationals who worked or resided abroad in malaria-endemic regions and subsequently returned to China. This distinguishes them from the broader term “migrants” (individuals who cross international borders for any duration or reason). This study does not include foreign-born migrants residing in China, as their travel histories and healthcare access patterns differ substantively from returned Chinese nationals.
Care‑seeking delay and diagnosis delay
According to World Health Organization guidelines, malaria diagnosis and treatment should occur within 24 h of symptom onset to minimize disease severity and reduce the risk of transmission [39]. However, achieving this recommendation in real-world clinical settings can be challenging. Thus, we adopted the operational definition suggested by Bastaki et al. defining overall delay as a period exceeding 4 days between symptom onset and diagnosis [40]. Consistent with previous studies [32], a delay in seeking care was defined as waiting longer than 3 days from symptom onset to first consultation. Diagnostic delay was defined as an interval exceeding 2 days from the patient’s first healthcare consultation to the date of confirmed malaria diagnosis (by microscopy or RDT) [40] (Fig. 2). But this approach has a limitation: it does not distinguish between delays attributable to clinician-initiated testing (e.g., failure to suspect malaria and order a diagnostic test) versus laboratory or reporting delays (e.g., time from test order to result availability). Distinguishing these components would require data on the date the diagnostic test was ordered and the date the result was reported to the clinician—information not available in the present study’s medical records. Therefore, the reported diagnostic delay represents a composite measure of both clinical and system-level factors.
Fig. 2.
Study definitions of delayed care-seeking and diagnosis for imported malaria
Data sources and variables
The details of each malaria patient recorded in the web-based China Information System for Disease Control and Prevention [41], were independently reviewed and confirmed by two researchers. The data collected included encompassed patient demographics (age and sex), countries visited, travel purpose, malaria infection history (all imported malaria cases in this study involved migrant workers frequently traveling to malaria-endemic areas and often reported previous malaria infections), dates of return to China, symptom onset, date of initial medical consultation, diagnosis dates, healthcare facility level accessed, pathogen species, and the GDP of destination cities in 2022 (Fig. 1B).
Data management and analysis
Prior to statistical analysis using SPSS software (version 28), data accuracy was rigorously verified. Variables are presented as mean ± standard deviation (SD) or median with interquartile range (IQR). Categorical data are expressed in terms of frequencies and percentages. Pearson's chi-square tests assessed differences in proportions, and two-sample t-tests compared means. Spearman's correlation analysis examined associations between diagnostic delay and 15 epidemiological variables. Multivariate logistic regression analysis was used to identify potential factors influencing delayed diagnosis, with statistical significance set at p < 0.05.
Characteristics of imported malaria cases, including temporal distribution, demographic features, travel motives, geographic regions visited, and Plasmodium species, were described. Additionally, intervals between symptom onset and first healthcare contact were analyzed to determine healthcare-seeking timeliness, and intervals between initial healthcare consultation and malaria diagnosis were assessed to evaluate diagnostic timeliness.
Results
General characteristics
Between January 1, 2012, and December 31, 2019, a total of 2098 cases of imported malaria were identified, all involving migrant workers. Table 1 provides an overview of patient characteristics according to Plasmodium species. The median age of patients was 44 years (IQR: 37–49), and most were male (97.8%, 2051/2098). Stratification by species revealed that 78.4% (1645/2098) were infected with P. falciparum, 12.6% (265/2098) with P. ovale, 4.8% (101/2098) with P. vivax, 3.6% (75/2098) with P. malariae, and 0.6% (12/2098) with mixed infections.
Table 1.
Epidemiological and clinical characteristics of imported malaria cases in Jiangsu Province, China, 2012–2019
| All n = 2098 |
P.
falciparum n = 1,645 |
P.
vivax n = 101 |
P.
ovale n = 265 |
P. malariae n = 75 |
Mixed n = 12 |
|
|---|---|---|---|---|---|---|
| Age (years), Median (IQR) | 44 (37–49) | 43 (36–48) | 45 (29–50) | 46 (42–50) | 46 (42–50) | 43 (39–45) |
| Gender | ||||||
| Male | 2051 (97.8) | 1609 (97.8) | 98 (97.0) | 260 (98.1) | 72 (96.0) | 11 (91.7) |
| Female | 47 (2.2) | 36 (2.2) | 3 (3.0) | 5 (1.9) | 3 (4.0) | 1 (8.3) |
| Region of travel | ||||||
| Sub-Saharan African countries | 1650 (78.6) | 1284 (78.1) | 79 (78.2) | 212 (80.0) | 64 (85.3) | 11 (91.7) |
| Non-SSA countries in Africa | 388 (18.5) | 312 (19.0) | 18 (17.8) | 47 (17.7) | 11 (14.7) | 0 (0.0) |
| Non-African countries | 60 (2.9) | 49 (3.0) | 4 (4.0) | 6 (2.3) | 0 (0.0) | 1 (8.3) |
| Season of returning | ||||||
|
December- February |
592 (28.2) | 473 (28.8) | 32 (31.7) | 63 (23.8) | 21 (28.0) | 3 (25.0) |
|
March- May |
477 (22.7) | 361 (21.9) | 17 (16.8) | 76 (28.7) | 22 (29.3) | 1 (8.3) |
|
June- August |
564 (26.9) | 445 (27.1) | 29 (28.7) | 71 (26.8) | 17 (22.7) | 2 (16.7) |
|
September- November |
465 (22.2) | 366 (22.2) | 23 (22.8) | 55 (20.8) | 15 (20.0) | 6 (50.0) |
|
Length of stay abroad (days), median (IQR) |
349 (180–631) | 339 (179–609) | 356 (177–656) | 376 (183–712) | 380 (244–649) | 372.5 (188–737) |
| History of malaria (any past diagnosis) | ||||||
| Yes | 1425 (67.9) | 1110 (67.5) | 70 (69.3) | 184 (69.4) | 52 (69.3) | 9 (75.0) |
| No | 673 (32.1) | 535 (32.5) | 31 (30.7) | 81 (30.6) | 23 (30.7) | 3 (25.0) |
History of malaria (any past diagnosis): Self-reported malaria infection at any time before the current episode; no specific time window was recorded
Sub-Saharan Africa (SSA) was identified as the most common region of origin for imported malaria cases, accounting for 78.7% (1650/2098) of patients. Among these, 30% (495/1650) arrived from Angola, and 29.5% (487/1650) arrived from Equatorial Guinea. The median duration of stay abroad was 349 days (IQR: 180–631 days), and 67.9% (1425/2098) reported a history of malaria infection (Table 1).
The number of imported malaria among migrant workers significantly rose from 2012 to 2019, increasing from 113 cases in 2012 to a peak of 386 in 2015. During the final three years of the study period, cases decreased slightly to approximately 214 annually (Fig. 3A). P. falciparum consistently remained the predominant species, comprising 77.5% (299/386) of cases in 2015 and 82.3% (158/192) in 2019 (Fig. 4A). Quarterly fluctuations in imported malaria cases between 2012 and 2019 are presented in Fig. 3B, showing the highest case count in the first quarter (December-February), which accounted for 28.2% (592 cases) of all reported cases. The highest monthly proportions for P. falciparum, P. ovale, and P. malariae occurred in January, at 13.3% (219/1645), 13.2% (35/265), and 17.3% (13/75), respectively (Fig. 4B).
Fig. 3.
Distribution of imported malaria cases in Jiangsu Province, China
Fig. 4.
Temporal trends of imported malaria by parasite species in Jiangsu Province, 2012–2019
Timing interval from onset to care seeking
The characteristics of health-seeking behaviours, categorized by the time interval between symptom onset and healthcare consultation, are detailed in Table 2. Patients sought care a median of one day after fever onset (IQR: 0–3 days). Most migrant workers with imported malaria sought healthcare within three days of symptom onset (74.6%; 1,566/2,098). Notably, nearly half of these patients (38.5%; 603/1566) accessed healthcare on the day after symptoms began.
Table 2.
Characteristics of the interval between noticing symptoms and diagnosis among imported cases
| Characteristics | Delayed care-seeking (> 3 days) |
Delayed diagnosis (> 2 days) |
||||||
|---|---|---|---|---|---|---|---|---|
| Yes (n = 532) |
No (n = 1566) |
χ2 | P-value | Yes (n = 316) |
No (n = 1,782) |
χ2 | P-value | |
| Gender | 0.498 | 0.480 | 0.144 | 0.704 | ||||
| Male | 518 (97.4) | 1533 (97.9) | 308 (97.5) | 1743 (97.8) | ||||
| Female | 14 (2.6) | 33 (2.1) | 8 (2.5) | 39 (2.2) | ||||
| Age, years | 1.327 | 0.515 | 2.171 | 0.338 | ||||
| ≤ 20 years | 1 (0.2) | 8 (0.5) | 0 (0.0) | 9 (0.5) | ||||
| 21—40 | 192 (36.1) | 541 (34.5) | 105 (33.2) | 628 (35.2) | ||||
| ≥ 41 | 339 (63.7) | 1017 (64.9) | 211 (66.8) | 1145 (64.3) | ||||
| Region of travel | 6.003 | 0.050 | 15.425 | 0.000 | ||||
| Sub-Saharan Africa | 427 (80.3) | 1223 (78.1) | 223 (70.6) | 1427 (80.1) | ||||
| Non-SSA countries in Africa | 84 (15.8) | 304 (19.4) | 78 (24.7) | 310 (17.4) | ||||
| Non-African countries | 21 (3.9) | 39 (2.5) | 15 (4.7) | 45 (2.5) | ||||
| Returning Year | 13.123 | 0.069 | 20.09 | 0.000 | ||||
| 2012 | 39 (7.3) | 74 (4.7) | 33 (10.4) | 80 (4.5) | ||||
| 2013 | 87 (16.4) | 235 (15.0) | 50 (15.8) | 272 (15.3) | ||||
| 2014 | 92 (17.3) | 248 (15.8) | 59 (18.7) | 281 (15.8) | ||||
| 2015 | 84 (15.8) | 302 (19.3) | 45 (14.2) | 341 (19.1) | ||||
| 2016 | 75 (14.1) | 221 (14.1) | 39 (12.3) | 257 (14.4) | ||||
| 2017 | 64 (12.0) | 158 (10.1) | 33 (10.4) | 189 (10.6) | ||||
| 2018 | 51 (9.6) | 176 (11.2) | 39 (12.3) | 188 (10.5) | ||||
| 2019 | 40 (7.5) | 152 (9.7) | 18 (5.7) | 174 (9.8) | ||||
| Returning month | 13.256 | 0.277 | 11.986 | 0.365 | ||||
| January | 75 (14.1) | 173 (11.0) | 29 (9.2) | 219 (12.3) | ||||
| February | 58 (10.9) | 130 (8.3) | 29 (9.2) | 159 (8.9) | ||||
| March | 30 (5.6) | 116 (7.4) | 21 (6.6) | 125 (7.0) | ||||
| April | 43 (8.1) | 100 (6.4) | 27 (8.5) | 116 (6.5) | ||||
| May | 43 (8.1) | 145 (9.3) | 25 (7.9) | 163 (9.1) | ||||
| June | 51 (9.6) | 162 (10.3) | 31 (9.8) | 182 (10.2) | ||||
| July | 43 (8.1) | 160 (10.2) | 25 (7.9) | 178 (10.0) | ||||
| August | 35 (6.6) | 113 (7.2) | 20 (6.3) | 128 (7.2) | ||||
| September | 38 (7.1) | 105 (6.7) | 31 (9.8) | 112 (6.3) | ||||
| October | 38 (7.1) | 128 (8.2) | 27 (8.5) | 139 (7.8) | ||||
| November | 40 (7.5) | 116 (7.4) | 28 (8.9) | 128 (7.2) | ||||
| December | 38 (7.1) | 118 (7.5) | 23 (7.3) | 133 (7.5) | ||||
| Healthcare facilities initially contacted | 27.665 | 0.001 | 434.674 | 0.000 | ||||
| Provincial healthcare institutions | 23 (4.3) | 45 (2.9) | 17 (5.4) | 51 (2.9) | ||||
| Municipal healthcare institutions | 166 (31.2) | 422 (26.9) | 55 (17.4) | 533 (29.9) | ||||
| County healthcare institutions | 282 (53.0) | 787 (50.3) | 73 (23.1) | 996 (55.9) | ||||
| Township health center | 41 (7.7) | 147 (9.4) | 55 (17.4) | 133 (7.5) | ||||
| Village clinic and other private agencies | 20 (3.8) | 165 (10.5) | 116 (36.7) | 69 (3.9) | ||||
| History of illness | 6.850 | 0.009 | 17.111 | 0.000 | ||||
| yes | 337 (63.3) | 1088 (69.5) | 183 (57.9) | 1242 (69.7) | ||||
| no | 195 (36.7) | 478 (30.5) | 133 (42.1) | 540 (30.3) | ||||
| Severe malaria | 0.012 | 0.913 | 6.810 | 0.009 | ||||
| Yes | 59 (11.1) | 171 (10.9) | 48 (15.2) | 182 (10.2) | ||||
| No | 473 (88.9) | 1395 (89.1) | 268 (84.8) | 1600 (89.8) | ||||
| Malaria species | 6.855 | 0.144 | 2.301 | 0.681 | ||||
| P. falciparum | 422 (79.3) | 1223 (78.1) | 251 (79.4) | 1394 (78.2) | ||||
| P. vivax | 17 (3.2) | 84 (5.4) | 14 (4.4) | 87 (4.9) | ||||
| P. ovale | 65 (12.2) | 200 (12.8) | 40 (12.7) | 225 (12.6) | ||||
| P. malariae | 23 (4.3) | 52 (3.3) | 11 (3.5) | 64 (3.6) | ||||
| Mixed infection | 5 (0.9) | 7 (0.4) | 0 (0.0) | 12 (0.7) | ||||
Timing interval from care seeking to diagnosis
The characteristics of diagnostic promptness, defined by the interval between seeking care and receiving a diagnosis, are presented in Table 2. Among the 2098 patients with imported malaria, most (84.9%; 1782/2098) were diagnosed within two days after seeking healthcare The proportion of patients experiencing delays of more than two days in obtaining a diagnosis has decreased in recent years, nevertheless 15% (316/2098) of patients still face such delays.
The association between the care-seeking delay and diagnostic delay
Between 2012 and 2019, trends in delays related to care-seeking and malaria diagnosis in Jiangsu Province did not differ significantly (χ2 = 6.092, p > 0.05). The highest proportions of delayed care-seeking and delayed diagnosis were observed in 2014 (Fig. 5). Significantly more patients sought healthcare within 3 days (83.3%, 263/316) compared to those seeking care after more than three days (16.8%, 53/316) (χ2 = 14.49, p < 0.05). Furthermore, as detailed in Table 3, the interval from symptom onset to healthcare-seeking showed a significant negative association with the interval from healthcare-seeking to diagnosis (r = − 0.052, p < 0.05).
Fig. 5.
Temporal trends in care-seeking delays and diagnostic delays among migrant workers diagnosed with imported malaria in Jiangsu Province, 2012–2019
Table 3.
Statistical analysis between delayed care-seeking and delayed diagnosis among migrant workers with imported malaria
| Factors | Total | Prompt diagnosis (≤ 2 days) | Delayed diagnosis (> 2 days) | Chi-square test | Spearman correlation test | ||
|---|---|---|---|---|---|---|---|
| χ2 | P-value | r-value | P-value | ||||
| Prompt care-seeking (≤ 3 days) | 1566 | 1303 (83.2) | 263 (16.8) | 14.49 | < 0.001 | −0.052 | 0.017 |
| Delayed care-seeking (> 3 days) | 532 | 479 (90) | 53 (10) | ||||
Factors associated with the diagnosis delay (> 48 h after care-seeking)
Table 4 presents the associations between various risk factors and diagnostic delay using a multivariable logistic regression model. Compared with diagnoses made in village and private clinics, care at county-level healthcare institutions was more likely to be associated with diagnostic delays (OR = 1.12, 95% CI 0.58–2.15). Additionally, imported malaria patients returning from non-African countries had a greater likelihood of delayed diagnosis than did those from SSA (OR = 1.41, 95% CI 0.66–3.02). Lower odds of delayed diagnosis were observed for patients with delayed care-seeking (> 72 h) (OR = 0.62, 95% CI: 0.44–0.88, P = 0.008), non–severe malaria (OR = 0.57, 95% CI 0.38–0.86, P = 0.007), and symptom onset after entry into China (OR = 0.46, 95% CI 0.31–0.69, P < 0.001).
Table 4.
Association (OR) between diagnosis delay and different risk factors by multivariable logistics regression model among migrant workers with imported malaria
| Variable | Odds ratio (95% CI) | P value |
|---|---|---|
| Intercept | ||
| Care-seeking behavior(Reference-Care-seeking within 3 days) | ||
| Care-seeking delay (> 3 days) | 0.62 (0.44, 0.88) | 0.008 |
| Severity of malaria (Reference-Severe malaria) | ||
| Non-severe malaria | 0.57 (0.38, 0.86) | 0.007 |
| Timing of symptom onset | 0.001 | |
| Pre-entry | Reference | |
| Within 1 week after entry | 0.47(0.13, 1.67) | 0.241 |
| From 1 week to 1 month after entry | 0.71(0.48, 1.04) | 0.077 |
| After 1 month | 0.46 (0.31, 0.69) | P < 0.001 |
| The level of the healthcare facility at which healthcare was initially sought | P < 0.001 | |
| Village clinics and private clinics | Reference | |
| Township healthcare institutions | 4.90 (2.55, 9.42) | P < 0.001 |
| County healthcare institutions | 1.12 (0.58, 2.15) | 0.741 |
| Municipal healthcare institutions | 0.20 (0.11, 0.37) | P < 0.001 |
| Provincial healthcare institution | 0.27(0.15, 0.52) | P < 0.001 |
| Region of travel | 0.003 | |
| Sub-Saharan African countries | Reference | |
| Non-SSA countries in Africa | 0.79(0.39, 1.62) | 0.520 |
| Non-African countries | 1.41(0.66, 3.02) | 0.373 |
| The GDP of the destination city | P < 0.001 | |
| Sub-Saharan African countries | Reference | |
| Second level | 2.74(1.88, 4.00) | P < 0.001 |
| Third level | 1.27 (0.88, 1.83) | 0.206 |
β, regression coefficient. According to the GDP in 2022 from large to small, the 13 cities in Jiangsu Province are divided into three level. The first level is the top four Suzhou, Wuxi, Nanjing and Nantong; the second level is the five cities: Changzhou, Xuzhou, Yangzhou, Yancheng and Taizhou; the third level is the four cities: Zhenjiang, Huai'an, Suqian, and Lianyungang. Statistical significance for multivariable results was defined as P < 0.05. Univariate analysis indicated that the following variables were not retained: sex (P = 0.494), age (P = 0.459), complications (P = 0.942), Plasmodium species (P = 0.943), Symptoms (P = 0.589), returning season (P = 0.056), duration of being abroad (P = 0.533), malaria infection history (P = 0.217), the interval between last infection and current infection (P = 0.533)
Discussion
This study examined the time intervals and related characteristics between diagnosis and seeking medical assistance among migrant workers diagnosed with imported malaria in Jiangsu Province from 2012 to 2019. The results revealed that compared with delays in establishing diagnoses, many patients experienced significant delays in seeking medical attention. Factors contributing to diagnostic delays included the severity of malaria infection, the specific travel location, the economic status of the cities visited, the onset timing of symptoms, and the quality of care at the initial health institution approached. Notably, seeking medical attention at an earlier stage was paradoxically associated with longer diagnostic delays. This indicates that patients with imported malaria frequently exhibit mild and nonspecific symptoms, potentially leading healthcare providers to underestimate the condition. These observations underscore an urgent need for heightened vigilance and improved response protocols among returning migrant populations and healthcare personnel to mitigate the risk of malaria reintroduction in previously malaria-free regions.
In examining the challenges of post-travel healthcare, it is evident that delays in accessing healthcare and in diagnosing imported malaria remain significant concerns across both developing and developed countries. However, direct comparisons of “diagnostic delay” between settings must be interpreted cautiously, because the composition of this delay differs substantially by health system structure, clinician awareness, and diagnostic capacity. In our study from China, despite a decline over the past decade, more than 25% (532/2098) of patients with imported malaria still experience delays exceeding 3 days in seeking care, and nearly 15% (316/2098) encountered diagnosis delays exceeding two days from first consultation to confirmed diagnosis. In France, patients typically arrived at hospitals about three days (IQR = 2–5) after symptom onset, but the median diagnostic interval from first medical advice to confirmation was less than one day [34]. This near-zero diagnostic delay after presentation likely reflects high clinician awareness of malaria among febrile returning travelers and rapid access to expert microscopy. In the United Kingdom, the median interval from fever onset to confirmation of malaria has remained stable at approximately four days over the past 25 years [42], suggesting persistent barriers at either the care-seeking or diagnostic stage. In Australia, median intervals from symptom onset to diagnosis were four days for P. falciparum and six days for P. vivax [43].
Critically, and indeed the awareness of malaria in a differential diagnosis algorithm for clinicians is a key determinant of whether diagnostic delay occurs before or after the first healthcare presentation. Without such awareness, even prompt care-seeking will not lead to timely diagnosis. These cross-country differences underscore that interventions must be tailored to the specific locus of delay in each setting: patient knowledge and care-seeking behavior in some contexts, versus clinician training and diagnostic algorithms in others. Delays in any part of this cascade can lead to severe outcomes, including death [44, 45], secondary transmission and potential reintroduction of malaria, underscoring the critical need for enhanced post-travel healthcare interventions, particularly among international migrant workers.
Our findings underscore that, overall, significant delays are more frequently associated with care-seeking behavior than with the diagnostic process itself. Notably, this investigation used a rigorous criterion for diagnostic delay (exceeding two days between initial healthcare visit and confirmed diagnosis). Despite this strict threshold, the median duration from first consultation to diagnosis among migrant workers in Jiangsu Province remained less than one day. However, this overall median masks important heterogeneity. Clinicians in China may be highly aware of malaria risk in returnees from Africa—who account for the majority of imported cases—but less aware of risk from other endemic regions, including the Arabian Peninsula and South Asia, where malaria transmission persists. This is clinically significant because Plasmodium vivax, which is more common in South Asia and the Middle East than P. falciparum, has a longer incubation period, may present with nonspecific or relapsing symptoms, and is less likely to be suspected by clinicians unfamiliar with regional epidemiology. The risk in returnees from countries such as Yemen, Saudi Arabia, Pakistan, India, and Myanmar should be explicitly emphasized in clinician training.
The “1–3–7” malaria surveillance and response strategy implemented in China has substantially improved suspected case reporting and established clear temporal guidelines for malaria diagnosis and confirmation [46]. This robust surveillance system serves as a critical intervention in itself, helping to prevent diagnostic delays [47–50]. Nevertheless, the effectiveness of this system depends on clinicians initially suspecting malaria—a prerequisite that may be weaker for migrants returning from non-African endemic areas. Therefore, targeted education for healthcare providers should move beyond Africa-centric messaging to include region-specific malaria risk profiles, with particular attention to vivax malaria and its atypical presentations.
Interestingly, our study indicated that early care-seeking was associated with longer diagnostic delays among migrant workers with imported malaria. This may occur because patients who seek healthcare early often present with milder symptoms, which can lead healthcare providers to overlook the possibility of malaria, thereby increasing the likelihood of delayed diagnosis [51–53]. Moreover, the patients themselves may misunderstanding the severity of their symptoms or mistaking them for the common flu, as the major symptoms of malaria are fever, headache, and muscle aches [54–56]. Furthermore, clinicians may fail to suspect or test for malaria, particularly in regions where malaria has been eliminated [57]. These findings underscore the need to strengthen clinicians’ awareness of imported malaria and their capacity for timely diagnosis and appropriate treatment, along with efforts to promote early care-seeking among migrant workers returning from malaria-endemic countries. Moreover, educational programs targeting migrant workers before their return could substantially reduce these initial delays by improving recognition of malaria symptoms.
Our study underscores that empowering primary healthcare institutions in managing imported malaria. Township and county healthcare institutions, although associated with diagnostic delays, play pivotal roles in early care-seeking behaviors among patients [58–60]. Therefore, enhancing capabilities at lower-level institutions could reduce diagnostic delays. The example of Purworejo is particularly instructive, demonstrating the effectiveness of community-based interventions in managing malaria even after local elimination [61, 62]. The integrated public health strategy employed by village malaria workers, which includes migration surveillance, rapid diagnostic testing, and coordination with community health centers for treatment, serves as a model for similar contexts.
Interestingly, returning migrant workers with imported malaria from non-African countries were more likely to experience diagnostic delays than those from African countries. The reason for this may be that the majority of patients with imported malaria from non-African countries are infected with P. vivax, which typically results in lower parasitemia and milder symptoms, as well as a lower mortality rate and a lower incidence of severe symptoms, compared with those with infection with P. falciparum [63, 64]. This can lead to underestimation of disease severity, resulting in delayed treatment and increased risk of transmission. However, this delay is particularly concerning given the potential for P. vivax to cause severe malaria and even death if not promptly and effectively treated [63, 65–67]. Given the wide distribution of vectors for P. vivax in China, particularly near bordering countries, there is an urgent need to address the potential reintroduction of this malaria species into regions previously declared malaria-free [16, 68].
Although this study investigated care-seeking and diagnostic delays of malaria infections among international migrant workers—a group that faces many health challenges yet is significantly understudied—several limitations should be considered when interpreting the results. First, the restricted sample size and the focus on a specific subgroup of migrant workers may not fully capture the diversity of migrant populations, thus potentially limiting the generalizability of our findings. Second, Although data used in this study originated from a comprehensive national monitoring database, which enhances its overall reliability, dependence on self-reported timelines for medical consultations inherently carries a risk of recall inaccuracies. Such inaccuracies may affect the precision of the reported intervals. Moreover, the method for calculating diagnostic delays, which did not account for time to the hour and only included the dates of symptom onset, diagnosis, and visits to health institutions or CDCs—may have led to an overestimation of the reported delays. This discrepancy suggests that the actual delays may be shorter than those documented, highlighting the need for a more precise measurement approach in future studies to better assess and address the health needs of this vulnerable population.
In addition, definition of diagnostic delay (≥ 2 days from first consultation to confirmed diagnosis) is a composite measure that does not allow us to distinguish between delays in clinician suspicion and test ordering versus laboratory processing and result reporting. This distinction is clinically important, as interventions to reduce each type of delay differ (e.g., provider education vs. laboratory infrastructure). Finally, we did not collect specific occupational data on migrant workers, even though occupation—such as night work, forest exposure, or remote-site labor—may influence malaria exposure risk and care-seeking patterns, and may differ systematically by gender.
Conclusions
This study provides important insights into the factors influencing delays in healthcare utilization and malaria diagnosis among migrant workers who returning to Jiangsu Province with imported malaria infections from 2012 to 2019. The results clearly demonstrate cause for concern regarding delayed healthcare-seeking behaviors among patients. In particular, the counterintuitive relationship between prompt medical consultation and increased diagnostic delay highlights healthcare providers’ tendency to miss mild and atypical presentations of imported malaria. Consequently, these findings reinforce the need for specifically tailored educational initiatives and training designed to enhance healthcare providers' diagnostic awareness and competence. Additionally, enhancing the diagnostic capabilities at primary care centers could facilitate earlier detection of malaria cases. Such initiatives are crucial to ensure timely and accurate diagnosis of malaria, thereby preventing its re-establishment in regions where it has previously been eliminated and safeguarding the health of this vulnerable population.
Acknowledgements
Special appreciation should be expressed to all the staffs in the local CDCs in Jiangsu Province.
Author contributions
TS: Formal analysis, Writing–original draft, Writing–review & editing. YC: Formal analysis, Writing–original draft, Writing–review & editing. KL: Formal analysis, Writing–original draft, Writing–review & editing. ZC: Investigation, Writing–review & editing. EX: Investigation, Writing–review & editing. YW: Investigation, Writing–review & editing. OM: Conceptualization, Formal analysis, Investigation, Writing–review & editing. JC: Conceptualization, Formal analysis, Investigation, Supervision, Writing–review & editing. GZ: Conceptualization, Formal analysis, Investigation, Supervision, Writing–review & editing. GL: Conceptualization, Supervision, Writing–review & editing.
Funding
This work was supported by the National Natural Science Foundation of China [Grant no. 72374178, 71904165]; Bill & Melinda Gates Foundation [Grant no. INV-075492]; the Open Project Program of Jiangsu Key Laboratory of Zoonosis [Grant no. R2208]; the Open Project Program of National Health Commission Key Laboratory of Parasitic Disease Control and Prevention and Jiangsu Provincial Key Laboratory on Parasite and Vector Control Technology [Grant no. wk023-007];the Jiangsu Provincial Health Commission (H2023004, and X202315); the Postgraduate Research and Practice Innovation Programme of Jiangsu Province [Grant no KYCX24-3852], Funding sources had no role in the design and conduct of the study; collection, managemant, analysis, and interpretation of the data; and preparation, review, or approval of the manscript.
Data availability
The data are not publicly available due to them containing information that could compromise research participant privacy and consent, but are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
This study was registered as a nationally funded research project aimed at improving the case management of patients with imported malaria (registration no. 72374178). Ethical approval was obtained from the Ethics Committee of the Medical College of Yangzhou University (approval no. YXYLL-2024–058).
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Taining Sha, Yuanyuan Cao and Kaixuan Liu have contributed equally to this study.
Contributor Information
Guoding Zhu, Email: zhuguoding@jipd.com.
Guangyu Lu, Email: guangyu.lu@yzu.edu.cn.
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Associated Data
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Data Availability Statement
The data are not publicly available due to them containing information that could compromise research participant privacy and consent, but are available from the corresponding author on reasonable request.