• View in gallery

    Distribution of imported Plasmodium falciparum malaria cases at the county level in Hubei Province from 2013 to 2018.

  • View in gallery

    Imported Plasmodium falciparum malaria country of acquisition in Hubei Province during 2013–2018.

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Epidemiology of Plasmodium falciparum Malaria and Risk Factors for Severe Disease in Hubei Province, China

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  • 1 Institute of Schistosomiasis Control, Hubei Provincial Center for Disease Control and Prevention, Wuhan, China;
  • 2 Department of Schistosomiasis and Endemic Diseases, Wuhan City Center for Disease Prevention and Control, Wuhan, China

This study aimed to describe the epidemiology of Plasmodium falciparum malaria and identify risk factors for severe disease in Hubei Province, China, using a case-based survey of retrospective data from 2013 to 2018. From 2013 to 2018, a total of 763 imported malaria cases were reported in Hubei Province; 69.2% (528/763) cases were caused by P. falciparum species. The proportion of malaria caused by P. falciparum increased from 66.7% in 2013 to 74.0% in 2018 (χ2 = 21.378, P < 0.05). Plasmodium falciparum malaria was reported in 77 counties of Hubei Province. The majority of imported P. falciparum cases originated from Africa (98.9%, 522/528); 9.7% (51/528) of patients infected with P. falciparum developed severe malaria. Three deaths (case fatality rate: 0.6%) were related to imported P. falciparum malaria. Risk factors for severe malaria were being female (odds ratio [OR] = 3.593, 95% CI: 1.003–12.874), age ≥ 50 years (OR = 2.674, 95% CI: 1.269–5.634), > 3 days between symptom onset and diagnosis (OR = 2.383, 95% CI: 1.210–4.693), and the first-visit medical institution at the township level or lower (OR = 2.568, 95% CI: 1.344–4.908). Malaria prevention should be undertaken among high-risk groups, infection with P. falciparum should be detected early to prevent severe disease and death, and healthcare providers in health facilities at the township level should be trained on early recognition of malaria.

INTRODUCTION

Malaria is one of the most common parasitic diseases in the world. According to the latest global estimates, in 2018, there were 228 million cases of malaria and 405,000 deaths.1 Infection with Plasmodium falciparum species is the most common cause of severe malaria.2 Importation of P. falciparum from endemic areas remains a challenge for malaria-free countries and countries working toward eliminating malaria. According to the WHO, 2–16% of imported P. falciparum infections caused severe malaria.3 With China working toward malaria elimination in 2020, no indigenous cases have been reported since 2017.4 However, the number of imported malaria cases in China has increased. Of 26,601 cases reported between 2011 and 2018, 93% were imported, with P. falciparum accounting for the majority of cases (58.3%, 15,501/26,601).57 From 2016 to 2018, the case fatality ratio of P. falciparum malaria was 5.05 per 1,000 cases (29 deaths in 5,745 P. falciparum imported cases).68

The number of imported P. falciparum malaria cases has been rising in Hubei Province (from 28 in 2010 to 105 in 2014).9 Plasmodium falciparum malaria is challenging because of its potential of resulting in severe cases and death. Reducing severe cases and deaths caused by imported falciparum malaria is one of the important goals in Hubei Province. To better understand and address this challenge, we conducted a case-based epidemiological survey on each imported P. falciparum malaria case in Hubei Province and described their epidemiological profiles using data from the China Information System for Disease Control and Prevention (CISDCP) and Information System for Parasitic Disease Control and Prevention (ISPDCP) collected between 2013 and 2018. In addition, we identified risk factors associated with severe malaria to help improve measures aimed at the prevention and management of P. falciparum malaria.

METHODS

Malaria case definition.

All P. falciparum malaria cases were confirmed through microscopy, rapid diagnostic tests, or polymerase chain reaction. In this study, we excluded cases of mixed infections of P. falciparum with other species from falciparum malaria cases. Only P. falciparum infections were included in the analysis. The definition of imported malaria was based on the technical scheme of malaria elimination in China definition, where an imported case is defined as an individual with malaria who traveled to a malaria-endemic area outside China within the previous month of disease onset. “Severe” P. falciparum malaria was defined based on previously described criteria2,10: 1) impaired level of consciousness, 2) prostration, 3) anemia (hemoglobin < 7 g/dL and packed cell volume < 20% in adults), 4) renal impairment (serum creatinine > 265 μmol/L), 5) pulmonary edema or acute respiratory distress syndrome, 6) hypoglycemia with blood glucose level < 2.2 mmol/L, 7) circulatory collapse or shock (systolic blood pressure < 80 mmHg in adults), 8) clinical jaundice, 9) hemoglobinuria, 10) acidosis (plasma bicarbonate < 15 mmol/L), and 11) hyperlactatemia (plasma lactate level > 5 mmol/L).

Data collection.

Data on individual P. falciparum cases reported at the county level in Hubei Province during 2013–2018 were obtained from the CISDCP and ISPDCP. Extracted patient characteristics included gender, age, nationality, purpose of travel, history of malaria infection, symptom onset before or after return to China, month of symptom onset, time from onset to diagnosis, and the administrative level of first-visit medical institution. Clinical information on severe malaria was obtained from attending clinicians after extraction of the medical records.

Statistical analysis.

Data were analyzed using SPSS version 16.0 (SPSS Inc., Chicago, IL). Categorical variables were reported as frequencies, whereas continuous variables were reported as median and interquartile range (IQR). For categorical variables, the differences in characteristics between groups were tested using χ2 test. Logistic regression analysis was used to identify risk factors associated with severe malaria, and to estimate associated odds ratios (ORs) and corresponding 95% CI. Only variables with P-values < 0.05 were considered to be statistically significant. ArcGIS version 10.0 (ESRI Inc., Redlands, CA) was used to present the geographical distribution of P. falciparum cases.

Ethical considerations.

This study was reviewed and approved by the Ethics Review Committee of the Hubei Provincial CDC. As the study was based on a retrospective review of disease reported data, informed consent was waived.

RESULTS

Epidemiological profiles of P. falciparum cases.

From 2013 to 2018, a total of 763 malaria cases were reported in Hubei Province. All the reported malaria cases were imported. Plasmodium falciparum was the most predominant species (69.2%, 528/763) of all reported malaria cases, with the highest peak occurring in 2014 (105 cases) and the smallest in 2017 (49 cases). The proportion of malaria cases caused by P. falciparum increased from 66.7% in 2013 to 74.0% in 2018 (χ2 = 21.378, P < 0.05). In 2018, a total of 127 imported malaria cases were reported, and 74.0% of them were identified as P. falciparum (Table 1). The number of counties with imported P. falciparum cases ranged from 31 to 41 per year; P. falciparum malaria cases were reported in 77 counties of Hubei (Figure 1). Of the patients with P. falciparum malaria, 9.7% (51/528) had severe malaria. The trend of proportion of patients with severe malaria from 2013 to 2018 was 12.8% (11/129), 8.6% (9/140), 11.0% (10/120), 9.7% (10/151), 8.2% (4/96), and 7.4% (7/127), respectively (Table 1). Three patients with P. falciparum malaria died (case fatality rate of 0.6%), and all of them were men who had returned from African countries. The times from onset of symptoms to diagnosis were 7, 8, and 4 days (Table 2).

Table 1

Descriptive statistics of P. falciparum in Hubei Province, China, 2013–2018

Characteristic201320142015201620172018Total
Total cases, N12914012015196127763
P. falciparum (% of total cases)86 (66.7)105 (75.0)91 (75.8)103 (68.2)49 (51.0)94 (74.0)528 (69.2)
Number of counties with imported P. falciparum cases31403541264077*
Severe cases of P. falciparum (% of total P. falciparum cases)11 (12.8)9 (8.6)10 (11.0)10 (9.7)4 (8.2)7 (7.4)51 (9.7)
Death number1100103

P. falciparum = Plasmodium falciparum.

County with imported P. falciparum cases for more than 1 year was counted only once.

Figure 1.
Figure 1.

Distribution of imported Plasmodium falciparum malaria cases at the county level in Hubei Province from 2013 to 2018.

Citation: The American Journal of Tropical Medicine and Hygiene 103, 4; 10.4269/ajtmh.20-0299

Table 2

Demographic characteristics of patients who died because of Plasmodium falciparum malaria

Case numberYearAge (years)GenderNationalityTravel purposeOrigin countryIllness and diagnose
Month of onsetTime from onset to diagnosis (days)The level of the first-visit health institution
1201330MaleChineseLaborCongo (Kinshasa)January7County hospital
2201441MaleChineseBusinessMozambiqueMarch8County hospital
3201728MaleChineseTranslatorNigeriaOctober4Private clinics

Region of infection acquisition for imported P. falciparum cases.

As shown in Figure 2, between 2013 and 2018, the 528 P. falciparum malaria cases imported into the Hubei Province were from 37 countries located in Africa, Asia, and South America. The largest number of imported cases was from Africa (98.9%, 522/528), mainly from Nigeria (13.1%, 69/528), Congo (Kinshasa) (12.3%, 65/528), Angola (12.1%, 64/528), Congo (Brazzaville) (6.3%, 33/528), Liberia (5.7%, 30/528), and Ghana (5.3%, 28/528). Of the 51 patients who had severe malaria, 98.0% (50/51) had traveled to Africa.

Figure 2.
Figure 2.

Imported Plasmodium falciparum malaria country of acquisition in Hubei Province during 2013–2018.

Citation: The American Journal of Tropical Medicine and Hygiene 103, 4; 10.4269/ajtmh.20-0299

Characteristics of patients with imported falciparum malaria in Hubei Province from 2013 to 2018.

Characteristics of patients with imported P. falciparum malaria are shown in Table 3. Men were predominant in both non-severe (97.1%, 463/477) and severe cases (92.2%, 47/51). The median age of non-severe and severe cases was 40 (30–46) years and 40 (28–49) years, respectively. There was a significant difference in the proportion of patients aged ≥ 50 years between non-severe and severe cases (χ2 = 5.179, P < 0.05). There were no significant differences between non-severe and severe cases with regard to gender, nationality, and travel purpose, symptom onset before or after return to China, and month of symptom onset (P > 0.05).

Table 3

Characteristics of patients with imported P. falciparum malaria in Hubei Province from 2013 to 2018

VariableAll (n = 528)Non-severe (n = 477)Severe (n = 51)χ2P-value
Gender, n (%)
 Male510 (96.6)463 (97.1)47 (92.2)2.0450.153
 Female18 (3.4)14 (2.9)4 (7.8)
Age (years)
 Median (IQR)40 (30–47)40 (30–46)40 (28–49)
Age-group (years), n (%)
 0–49458 (86.7)419 (87.8)39 (76.5)5.1790.023
 ≥ 5070 (13.3)58 (12.2)12 (23.5)
Nationality, n (%)
 Chinese515 (97.5)465 (97.5)50 (98.0)0.0001.000
 Africa13 (2.5)12 (2.5)1 (2.0)
Travel purpose, n (%)
 Labor479 (90.7)434 (91.0)45 (88.2)0.1520.697
 Other*49 (9.3)43 (9.0)6 (11.8)
History of malaria infection, n (%)
 Yes319 (60.4)296 (62.1)23 (45.1)5.5390.019
 No209 (39.6)181 (37.9)28 (54.9)
Symptom onset, n (%)
 Before return to china61 (11.6)56 (11.7)5 (9.8)0.1690.681
 After return to china467 (88.4)421 (88.3)46 (90.2)
Months of symptom onset, n (%)
 1–2115 (21.8)104 (21.8)11 (21.6)0.0010.969
 3–12413 (78.2)373 (78.2)40 (78.4)
Time from onset to diagnosis
 Median (IQR)4 (2–6)3 (3–6)5 (3–9)
Group (days), n (%)
 0–3256 (48.5)242 (50.7)14 (27.5)10.0000.002
 > 3272 (51.5)235 (49.3)37 (72.5)
Administrative level of first-visit medical institution, n (%)
 Township level or lower108 (20.5)88 (18.4)20 (39.2)12.2120.000
 County level or higher420 (79.5)389 (81.6)31 (60.8)

IQR = interquartile range.

Other, including business and study.

The median time from onset to diagnosis was 3 days (IQR = 3–6 days) for non-severe cases and 5 days (IQR = 3–9 days) for severe cases; there was a significant difference in the proportion of cases with > 3 days from onset to diagnosis between non-severe and severe cases (χ2 = 10.000, P < 0.05). There was a difference in the history of malaria infection (χ2 = 5.539, P < 0.05), and the proportion of first visits to medical institutions at a township level or lower (χ2 = 12.212, P < 0.05) (Table 3).

Risk factors for severe malaria.

Being female (OR = 3.593, 95% CI: 1.003–12.874), age ≥ 50 years (OR = 2.674, 95% CI: 1.269–5.634), > 3 days between symptom onset and diagnosis (OR = 2.383, 95% CI: 1.210–4.693), and the first-visit medical institution at the township level or lower (OR = 2.568, 95% CI: 1.344–4.908) were identified as risk factors for severe malaria. However, no significant association was found between severe cases and nationality, purpose of travel, no history of malaria infection, symptom onset before return to China, and month of symptom onset in January and February (P > 0.05) (Table 4).

Table 4

Factors associated with the risk of severity in Plasmodium falciparum malaria cases from 2013 to 2018

VariableOdds ratio (95% CI)P-value
Gender, female3.593 (1.003, 12.874)0.049
Aged ≥ 50 years2.674 (1.269, 5.634)0.010
Nationality, Chinese2.082 (0.202, 21.448)0.538
Travel purpose, labor0.740 (0.250, 2.190)0.587
No history of malaria infection1.633 (0.888, 3.003)0.115
Symptom onset before return to china0.696 (0.256, 1.891)0.477
Month of symptom onset in January and February1.106 (0.596, 2.053)0.750
Time from onset to diagnosis > 3 days2.383 (1.210, 4.693)0.012
First-visit medical institution at the township level or lower2.568 (1.344, 4.908)0.004

DISCUSSION

The present study has identified changes in epidemiological characteristics of P. falciparum malaria imported over the past 6 years into Hubei Province, China. Plasmodium falciparum was the most predominant species imported. This situation is similar to the distribution of P. falciparum in China.4,5,11 Men and middle-aged adults constituted most P. falciparum malaria cases during the study period. This study indicated that travel to malaria-endemic countries for work-related purposes might be the most important cause associated with imported malaria cases in Hubei. The main source of imported P. falciparum malaria in Hubei was Africa, where P. falciparum is highly endemic. Previous studies have indicated that the incidence of malaria was high among Chinese workers who had worked in African countries.1216 Overseas workers generally lack immunity to P. falciparum species which is endemic in the new work area.17 In addition, workers tend to have insufficient knowledge and awareness regarding the risk of malaria infection.18 Thus, these workers should receive pretravel health advice as a matter of priority. Moreover, appropriate preventive measures, such as use of antimalaria chemoprophylaxis and personal protection measures against mosquito bites, should be enforced.

No indigenous cases of P. falciparum malaria have been reported since 1963 in Hubei Province. The first imported P. falciparum case was reported in 1999.19 During 2013–2018, imported P. falciparum malaria cases were reported in 77 counties of Hubei. In addition, the threat of P. falciparum drug resistance remains a problem for malaria treatment.20,21 Global warming can cause latitudinal and altitudinal shifts in vector distributions, thereby changing the risk of malaria.22 Imported P. falciparum malaria will continue to pose a challenge for eliminating malaria. Therefore, intensifying proactive surveillance systems and ensuring that the risk of transmission of P. falciparum is detected early are paramount to malaria elimination.4,23

Our analyses have indicated that four factors were associated with severe cases of P. falciparum malaria. The correlation between female gender and severe malaria found in this current study has not been reported in previous studies.2426 The reasons for this result were likely due to the small sample size. Age ≥ 50 years was a risk factor for severe malaria among imported P. falciparum cases. Previous studies have indicated that older age is a risk factor for severe imported P. falciparum malaria.2628 This finding should prompt clinicians to advice travelers aged ≥ 50 years on malaria prevention, and highlights the need for early diagnosis and treatment for patients with early symptoms of malaria. Time delay of > 3 days between onset and diagnosis was associated with an increased risk of severe malaria in this study. Seringe et al.29 have reported that a time lapse of 4–12 days between the onset of symptoms and diagnosis of malaria was a risk factor for severe malaria. Some studies have also indicated that delays in diagnosis contribute to severe malaria.30,31 Early diagnosis is crucial for malaria control and treatment.

The first-visit medical institution at the township level or lower is likely to contribute to high numbers of severe malaria cases. This finding might be due to either lack of perceived risk and skills, or insufficient training provided by medical institutions at township and lower levels. Ding et al.32 have reported that the capacity for malaria diagnosis at institutions at township or lower levels was insufficient. Regular training and supervision of malaria diagnosis–related skills at institutions at township levels or lower should be emphasized in Hubei Province.

Lai et al.14 found higher case mortality rates in imported P. falciparum cases during January and February, a period that includes the Chinese New Year celebrations. Delayed presentation to medical services and fewer medical staff on duty during the holiday might contribute to delayed diagnosis that results in a more severe malaria course. However, in our study, there was no significant association between risk of severe malaria and symptom onset in January and February.

Inability to assess factors such as educational level, parasite genetics, access to appropriate treatment, and antimalarial drug resistance, which are related to clinical outcomes of P. falciparum malaria, is considered a major limitation in this study. Future research should examine the contribution of these factors to the epidemiological profile of imported malaria cases in Hubei Province, China.

In conclusion, P. falciparum was the predominant imported plasmodium species. Imported P. falciparum malaria cases were reported in 77 counties of Hubei. Severe disease accounted for 9.7% of all P. falciparum cases. Risk factors for severe malaria were female gender, age ≥ 50 years, > 3 days between symptom onset and diagnosis, and the first-visit medical institution at the township level or lower. This research can further enrich knowledge and help provide valuable reference for the effective management of these cases in the future.

Acknowledgment:

We thank all the staff in the county CDC in Hubei Province.

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    Zhang L, Feng J, Zhang SS, Xia ZG, Zhou SS, 2018. The progress of national malaria elimination and epidemiological characteristics of malaria in China in 2017 [article in Chinese]. Chin J Parasitol Parasit Dis 36: 201209.

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    • Export Citation
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    • Export Citation
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    • Export Citation
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    Wu HM, Fang ZQ, Zhao D, Chen YL, Liu CG, Liang X, 2017. A study on the epidemiological characteristics and infectious forecast model of malaria at Guangzhou airport among Chinese returnees from Africa. Malar J 16: 275.

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    • Export Citation
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    Liu YB, Hsiang MS, Zhou HY, Wang WM, Cao YY, Gosling RD, Cao J, Gao Q, 2014. Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu province, 2001–2011. Malar J 13: 29.

    • Search Google Scholar
    • Export Citation
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    Lai SJ 2016. Plasmodium falciparum malaria importation from Africa to China and its mortality: an analysis of driving factors. Sci Rep 6: 39524.

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    • Export Citation
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    Zhang SS, Feng J, Zhang L, Ren X, Geoffroy E, Manguin S, Frutos R, Zhou SS, 2019. Imported malaria cases in former endemic and non-malaria endemic areas in China: are there differences in case profile and time to response? Infect Dis Poverty 8: 61.

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    • Export Citation
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Author Notes

Address correspondence to Huaxun Zhang or Si Liu, Institute of Schistosomiasis Control, Hubei Provincial Center for Disease Control and Prevention, Zhuodaoquan North Road 35, Wuhan 430079, China. E-mails: huaxunzhang0707@163.com or liusi163@163.com

Financial support: This study was supported by the CDC of the Hubei Provincial Health and Family Planning Commission (Grant no. WJ2016J-037).

Authors’ addresses: Jing Xia, Dongni Wu, Hong Zhu, Lingcong Sun, Wen Lin, Kaijie Li, Juan Zhang, Lun Wan, Huaxun Zhang, and Si Liu, Institute of Schistosomiasis Control, Hubei Provincial Center for Disease Control and Prevention, Wuhan, China, E-mails: xiaj0608@163.com, wudongnitiancai@hotmail.com, whzh2005@aliyun.com, 54996685@qq.com, 5078294@qq.com, 7856151@qq.com, 371092511@qq.com, 526177817@qq.com, huaxunzhang0707@163.com, and liusi163@163.com. Kai Wu, Department of Schistosomiasis and Endemic Diseases, Wuhan City Center for Disease Prevention and Control, Wuhan, China, E-mail: cage2008@qq.com.

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