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  • Scoping Review
  • Open Access

Imported parasitic diseases in mainland China: current status and perspectives for better control and prevention

Infectious Diseases of Poverty20187:78

https://doi.org/10.1186/s40249-018-0454-z

  • Received: 12 February 2018
  • Accepted: 19 June 2018
  • Published:

Abstract

Background

The high prevalence of parasitic diseases leads to millions of deaths and disabilities each year in developing countries. China has also been greatly affected by parasitic infections, including filariasis, leishmaniasis, malaria, schistosomiasis, and soil-transmitted nematodosis. However, the situation in China improved dramatically after comprehensive parasitic disease control efforts were strengthened, leading to the elimination of filariasis in 2006 and to significant control over other diseases. However, imported parasitic disease cases are inevitable, and such cases have increasingly been reported as a result of enhanced globalization and international or regional cooperation. These imported diseases represent a major obstacle to the elimination of several parasitoses, such as malaria.

Main text

This paper reviews imported cases of parasitic diseases in mainland China, particularly malaria and schistosomiasis, based on data reported separately by the Chinese annual reports and from other published papers. We summarize the new challenges that face parasitic disease control efforts in mainland China and perspectives regarding better control. We argue that both the provision of professional education and updated training for medical care personnel and the management and surveillance of people entering China are essential. We recommend that Chinese migrant workers should be considered a priority group for health education and that public awareness of imported diseases should be emphasized. Furthermore, we underscore the importance of investigating the distribution of introduced/potential vectors, parasite susceptibility, and improvements in diagnostic techniques and drug stocks.

Conclusions

Imported cases have become the main challenge to the elimination of several parasitoses, such as malaria and schistosomiasis, in mainland China. China should act to meet these challenges, which are closely associated with national biological safety.

Keywords

  • Parasitic diseases
  • Imported disease
  • China

Multilingual abstract

Please see Additional file 1 for translations of the abstract into the five official working languages of the United Nations.

Background

Parasitic infections are considered diseases of poverty and are highly prevalent in developing countries, leading to millions of deaths and disabilities each year [1, 2]. Although humans in China previously suffered significantly from parasitic diseases [2], the rapid economic growth over the past six decades has led to the increased allocation of resources toward the control of parasitic diseases. Consequently, the status of parasitic diseases in China has improved considerably (Table 1) [39]. For instance, more than 30 million cases of lymphatic filariasis, a highly disfiguring infectious disease, were reported in 16 provinces/autonomous regions of mainland China during the 1950s. These cases included 5.4 million patients with severe disease who presented with signs such as elephantiasis, chyluria, hydroceles, and vaginal infection. After long-term efforts, China became the first developing country in the world to eliminate this parasitic disease in 2006 [3].
Table 1

Previous and current status of the main parasitic diseases in mainland China

Parasitic diseases

Estimated no. of patients

Endemic provinces/autonomous regions

Transmission vector

Transmission route

Elimination program

Past (million)

Present

Past

Present a

Filariasis

30 (1950s)

0 (2016)

16

0

Mosquito

Mosquito bites

Done

Leishmaniosis

0.53 (1950s)

400 ± annually b

16

7 c

Sandfly

Sandfly bites

Almost done

Malaria

30 (1960s)

3321 (2016)

24

2 d

Anopheline mosquito

Mosquito bites

Ongoing

Schistosomiasis

11.6 (1950s)

54 454 (2016)

12

7 e

Oncomelania hupensis

Infested water contact

Starting

Echinococcosis

0.38 (2004)

40 845 (2015)

21

9 f

Fecal-oral route

Soil-transmitted nematodosis

536 (1990)

3.12% (2013)

31

31 g

Fecal-oral route/skin

aPresent endemic province/autonomous regions: local infections

bThe prevalence of leishmaniosis in mainland China is not available; only annual new cases were found

cSeven provinces/autonomous regions: Xinjiang, Gansu, Sichuan, Shanxi, Shaanxi, Neimenggu, Henan

dThree provinces/autonomous regions: Yunnan, Tibet

eSeven provinces/autonomous regions: Hunan, Jiangxi, Anhui, Hubei, Yunnan, Sichuan, Jiangsu

fNine provinces/autonomous regions: Tibet, Qinghai, Neimenggu, Xinjiang, Shanxi, Gansu, Ningxia, Yunnan, Sichuan

gData for Hong Kong, Macao and Taiwan Province were not available and are not included

Leishmaniasis, or kala-azar disease, has been classified as one of the most neglected tropical diseases by the World Health Organization (WHO) and represents a serious global health burden [4]. Although China reported approximately 0.53 million patients with leishmaniasis in 16 provinces/autonomous regions during the early 1950s, this disease was nearly eliminated in 1958 by the large-scale treatment of infected dogs (reservoir hosts) and the use of antiparasitic drugs [4]. Approximately 400 new cases of this zoonotic parasite occur annually in China [5].

Malaria, which caused 445 000 deaths in 2016, is the most devastating parasitic disease worldwide [10]. More than 24 million people in 24 provinces/autonomous regions of mainland China were estimated to suffer from malaria in the 1970s [11]. Following unrelenting efforts, a Chinese national malaria prevention and control program has progressed to the next stage, the Action Plan of China Malaria Elimination (2010–2020) [12]. Accordingly, malaria elimination has transformed from a concept to a fact, as demonstrated by the cases reported in mainland China during 2016: approximately 99.9% of the cases (3317 of 3321) were imported, whereas only 0.1% of the cases (3 of 3321) involved local infections in border regions such as Yunnan and Tibet [8].

Schistosomiasis is another debilitating parasitic disease with severe symptoms, such as hepatosplenomegaly, liver fibrosis, and upper gastrointestinal bleeding. In the 1950s, schistosomiasis was estimated to affect 11.6 million people in mainland China, and the intermediate snail host, Oncomelania hupensis, is found in 14.3 billion square meters across 12 provinces/autonomous regions, leading to an infection risk for more than 100 million people who reside in these areas [7]. However, the number of schistosomiasis cases decreased to 54 454, and the schistosome infection rates of both humans and livestock decreased to less than 1% throughout all 451 endemic counties in 2016 [13]. Accordingly, China is currently working toward the elimination of schistosomiasis and is expected to soon fulfill the goals outlined by the Healthy China 2030 Plan.

Echinococcosis, a natural-focal disease, is costly and complicated to treat because the treatment regimen generally involves extensive surgery followed by prolonged and intensive drug therapy. Estimates suggest that although 380 000 persons acquired this infection in 2004 [14], the number of cases decreased to 40 845 in 2015 following the implementation of the Action Plan for Echinococcosis Control (2010–2015) [9]. Nevertheless, echinococcosis remains challenging in China, and the control program should be continued and expanded.

Soil-transmitted helminthiasis (i.e., infections with roundworms, pinworms, whipworms, and hookworms) is widely distributed throughout China. The prevalence of this condition has been extremely high, with positive rates of up to 53.67% (536 million infections) among individuals tested during the first national survey of human parasitic diseases in China conducted in 1990 [14]. A comprehensive surveillance system and integrated control campaign launched in 2006 have led to a steady and apparent decline in nematodiasis, with average infection rates of 20.88, 18.93, 16.59, 13.30, 11.25, 9.67, 6.90, and 3.12% in 2006, 2007, 2008, 2009, 2010, 2011, 2012, and 2013, respectively [6]. These data demonstrate the remarkable achievements in local parasitic diseases control throughout China and indicate that these efforts toward the prevention and control of parasitic diseases should be continued.

However, new imported cases of parasitic diseases are inevitable and will likely become increasingly common due to enhanced globalization as well as international and regional communication and cooperation. Estimates suggest that as many as 244 million people worldwide were living outside their countries of birth in 2015 [15]. Travel exchanges between different environments play a crucial role in the successful management of parasitic diseases in migrant receiving countries, particularly in cases in which vectors (e.g., snails, mosquitoes) are also present in China and may thus induce local infections.

Main text

Review of imported parasitic diseases in mainland China

Figure 1 presents the entire literature review process. First, annual reports from the Chinese Center for Disease Control and Prevention (published in Malaria Situation in the People’s Republic of China and Endemic status of schistosomiasis in People’s Republic of China) were examined. Relevant data (reported province/autonomous regions, source country/province, parasite species) were extracted, processed, and analysed using Excel 2013 (Microsoft Corp., Redmond, WA, USA). Then, a systematic literature search was conducted in CNKI (http://cnki.net/), Wanfang (http://new.wanfangdata.com.cn/) and PubMed (https://www.ncbi.nlm.nih.gov/pubmed) about the imported parasitic diseases in mainland China. The retrieval time: From Jan 1980 to Jan 2018. The keywords “imported and (Malaria or Schistosomiasis or Trypanosomiasis or Loaiasis or Echinococcosis or Soil-transmitted helminthiasis or Filariasis or Leishmaniosis) and China”. All identified papers were screened. Inclusive criteria: (1) Studies that were published from Jan 1980 to Jan 2018; (2) Studies that were published in Chinese or English; (3) Studies that focused on imported parasitic diseases in mainland China. Exclusion criteria: (1) Cases containing overlapping data; (2) Cases without details (age, sex, occupation, travel history, diagnostic process, reported province/autonomous regions, source country/province, parasite species). Relevant data were extracted, processed, and analysed using Excel 2013.
Fig. 1
Fig. 1

Overall process of reviewing Chinese annual reports and other literature. a Chinese annual reports: annual Malaria Situation in the People’s Republic of China collected for Chin J Parasitol Parasit Dis (1988–2016; 2001 was not available) and annual Endemic status of schistosomiasis in People’s Republic of China collected from Chin J Schisto Control (1999–2016). b Two (largest) Chinese databases: CNKI and Wanfang; one English database search engine: PubMed

Current status of imported parasitic diseases

Imported malaria

Although malaria was once highly prevalent in 24 provinces/autonomous regions of China, local infections were reported in only Yunnan and Tibet in 2016 [8, 12]. However, except for Tibet, the remaining 30 provinces/autonomous regions in mainland China reported imported cases in the latest Chinese annual report (2016) [8]. The top five provinces/autonomous regions in terms of reported cases imported from abroad (i.e., Chinese residents who acquire an infection abroad and return to China or foreign travellers who acquire an infection in their own country before traveling to China) were Yunnan, Guangxi, Jiangsu, Sichuan, and Henan during 2011 and 2016. The five main source countries of these malarial infections were Myanmar, Ghana, Angola, Equatorial Guinea, and Nigeria during 2011 and 2014 (Table 2) [8, 1620]. During 2011 and 2016, Plasmodium falciparum malaria was most common, causing 61.5% of cases, followed by P. vivax malaria (27.8%), P. ovale malaria (5.1%) and P. malariae malaria (1.4%) (Table 3) [8, 1620]. One case of P. knowlesi malaria was reported in 2014 [19]. Countries that share borders with China, such as Myanmar, continue to suffer intensely from malaria, and this fact presents an obstacle to the elimination of local infections in Chinese border regions [8]. Accordingly, a few cases of domestically mobile (i.e., imported inter- and intra-provincially) infection have been reported annually over the past five years [8, 1620].
Table 2

Five main reported provinces/autonomous regions in mainland China and source countries associated with cases of malaria imported from abroad (Chinese annual report) from 2011 to 2016

Year

No. of reported provinces/autonomous regions

No. of cases from five main reported provinces/autonomous regions

No. of cases from five main source countries

YN

GX

JS

SC

HN

Myanmar

Ghana

Angola

Equatorial Guinea

Nigeria

2016

30

410

305

307

327

198

2015

31

585

236

405

290

184

2014

30 a

486

184

355

264

216

488

188

278

289

330

2013

30 b

513

1251

341

234

194

608

1345

442

296

217

2012

29 c

679

219

198

148

150

764

241

151

233

197

2011

25

1086

111

357

172

184

1148

88

277

199

243

Total

3759

2306

1963

1435

1126

3008

1862

1148

1017

987

YN: Yunan; GX: Guangxi; JS: Jiangsu; SC: Sichuan; HN: Henan

Mainland China has 31 provinces (Hong Kong, Macao, and Taiwan Province not included)

aExcept for Neimenggu; b except for Tibet; c except for Tibet and Qinghai

Table 3

Numbers of cases (Chinese annual report) of each type of malaria imported from abroad in mainland China from 2011 to 2015

Diagnosis year

No. of cases

P. falciparum malaria

P. vivax malaria

P. ovale malaria

P. malariae malaria

Mixed infection

Unidentified type

P. knowlesi malaria

No.

%

No.

%

No.

%

No.

%

No.

%

No.

%

No.

%

2016

3317

2158

65.1

709

21.4

311

9.4

64

1.9

61

1.8

14

0.4

0

0.0

2015

3248

1991

61.3

851

26.2

272

8.4

70

2.2

47

1.5

17

0.5

0

0.0

2014

3021

1876

62.1

798

26.4

231

7.7

52

1.7

44

1.5

19

0.6

1

0.0

2013

4042

2899

71.7

859

21.2

133

3.3

51

1.3

65

1.6

35

0.9

0

0.0

2012

2474

1403

56.7

901

36.4

28

1.1

28

1.1

39

1.6

75

3.0

0

0.0

2011

2974

1414

47.6

1183

39.8

0

0.0

0

0.0

99

3.3

278

9.4

0

0.0

Total

19 076

11 741

61.5

5301

27.8

975

5.1

265

1.4

355

1.9

438

2.3

1

0.0

The literature reports of imported malaria cases are not fully consistent with those reported by the Chinese annual report [21111]. For instance, Yunnan Province reported most of the imported cases in the past consecutive three annual reports (2014–2016), but Hubei Province reported most of the imported cases in the other literature reports from 1986 to 2017, and the proportion of P. falciparum malaria was higher in literature reports (75%) than in the Chinese annual report (65% in 2016). Both the literature and Chinese annual reports described similar source countries, and both ranked Myanmar first. Among the 113 imported malaria cases from literature from 1986 to 2017, 108 (95.6%) were identified in men; this was likely because 73 of the cases (64.6%) involved migrant workers from Africa or Southeast Asia from 2000 to 2017. Twelve deaths (10.6%) were reported and attributed to misdiagnosis or delayed treatment from 1989 to 2013. Only a few domestically mobile cases were reported, and all occurred at least ten years ago [112124].

Imported schistosomiasis

Of the five main types of schistosomiasis, only schistosomiasis japonica is prevalent in China [7]. Transmission of this disease has already ceased in six (Sichuan, Zhejiang, Shanghai, Fujian, Guangdong, and Guangxi) of the original 12 endemic provinces/autonomous regions, but cases continue to occur in Yunnan, Jiangsu, Hubei, Anhui, Hunan, and Jiangxi [7, 125]. Therefore, schistosomiasis japonica remains domestically mobile in China. A summary of imported cases of schistosomiasis (Chinese annual reports) in mainland China from 2001 to 2016 is provided in Additional file 2 [13, 126140]. Only four cases of schistosomiasis mansoni imported from abroad were reported in Beijing (2008, 2010) and Zhejiang (2013, 2015), and two cases of schistosomiasis haematobia were reported in Zhejiang in 2016. Overall, 123 chronic and 65 acute imported cases of schistosomiasis japonica were reported during 2011 and 2016 and were mainly distributed in Zhejiang and Shanghai.

The relevant literature from 1999 to 2016 is displayed in Table 4. Nine schistosomiasis cases imported from abroad have been reported, of which eight involved Chinese migrant workers returning from Africa (Angola, Nigeria and Tanzania) and the ninth involved a businessman returning from Ghana [141148]. Twenty domestically mobile cases were reported in mainland China [149155], fifteen of which involved transmission from non-endemic or transmission-disrupted areas to endemic areas wherein patients were infected upon returning to their hometowns. The remaining five patients were migrant workers from endemic areas in Zhejiang (a transmission-disrupted province).
Table 4

Domestically mobile cases of schistosomiasis and those imported from abroad in mainland China from 1999 to 2016 (literature-based)

Diagnosis year

Reported province

Sex

Age

Source country/province

Activity/occupation

Diseases c

Ref

2016

Fujian

1 M

30

Angola

Migrant worker a

Sh

141

2015

Shandong

1 M

38

Angola

Migrant worker a

Sh

142

2015

Zhejiang

1 M

52

Nigeria

Migrant worker a

Sh

143

2015

Zhejiang

1 M

53

Nigeria

Migrant worker a

Sh

144

2013

Zhejiang

1 M

46

Nigeria

Migrant worker a

Sm

145

2012

Shanxi

1 M

36

Angola

Migrant worker a

Sh

146

2012

Fujian

1 M

25

Ghana

businessman

Sh

147

2011

Henan

1 M

40

Angola

Migrant worker a

Sh

148

2011

Henan

1 M

33

Tanzania

Migrant worker a

Sh

148

2009

Jiangsu

1 M 1F

9

Jiangxi

Student

Sj

149

2005

Guizhou

8 M

30–54

Hubei/Hunan

Catch birds

Sj

150

2005

Zhejiang

1 M

18

Anhui

Migrant worker b

Sj

151

2004

Zhejiang

1 M

49

Hubei

Migrant worker b

Sj

151

2004

Zhejiang

1F

41

Sichuan

Migrant worker b

Sj

152

2003

Zhejiang

1 M

36

Anhui

Migrant worker b

Sj

153

2003

Zhejiang

1 M

24

Hubei

Migrant worker b

Sj

153

2000

Guangdong

1 M

19

Hunan

Shipbuilder

Sj

154

1999

Zhejiang

1 M

39

Anhui

Fish farming

Sj

155

M Male, F Female

aMigrant worker to Africa; bMigrant worker to another province/autonomous regions in mainland China

cSh: Schistosomiasis haematobia; Sm: Schistosomiasis mansoni; Sj: Schistosomiasis japonica

Other imported parasitic diseases

A literature-based list of imported parasitic diseases other than malaria and schistosomiasis in mainland China is presented in Table 5 [156161].
Table 5

Abroad-imported cases of other parasitic diseases in mainland China (literature-based)

Diagnosis year

Reported province/autonomous regions

Sex

Age

Source country

Activity/occupation

Diseases

Ref

2017

Fujian

F

41

Kenya/Tanzania

Travel

Trypanosomiasis

156

2015

Beijing

M

49

Congo

Migrant worker

Loaiasis

157

2015

Beijing

M

28

Nigeria

Cartwright

Loaiasis

158

2015

Beijing

M

49

Congo

Migrant worker

Loaiasis

158

2014

Jiangsu

M

45

Gabon

Migrant worker

Trypanosomiasis

159

2013

Beijing

M

33

Gabon/Cameroun

Migrant worker

Loaiasis

158

2012

Beijing

M

25

Gabon

Engineer

Loaiasis

158

2012

Beijing

M

23

Cameroun

Translator

Loaiasis

158

2008

Zhejiang

M

45

Gabon

Farming

Loaiasis

160

2008

Zhejiang

M

45

Gabon

Migrant worker

Loaiasis

161

M Male, F Female

Perspectives for better control and prevention

Estimates suggest that as many as 244 million people worldwide are living outside their country of birth [15], and travel between different environments plays a crucial role in the management of parasitic diseases in countries that receive migrants. In other words, imported parasitic diseases are unavoidable. The China Africa Project, which aimed to assist with infrastructure construction, has led to a dramatic increase in the number of migrant workers who have moved to Africa since the 1970s [7]. In addition, increasing numbers of Chinese companies, particularly the communications industries, have established overseas subsidiaries over the past decade to capitalize on the African market. Current estimates indicate that more than 1 million Chinese live in Africa [7]. These individuals lack knowledge about self-protection and are at risk of acquiring schistosomiasis while swimming in unclean water, developing malaria after failing to protect against mosquito bites, or contracting other parasitic infections by eating infected food. This situation is exacerbated by a failure to report their travel history to a physician. Because many physicians in China are somewhat unfamiliar with parasitology, this omission presents an obstacle to a correct diagnosis [162]. The Belt and Road Initiative, proposed in 2013 by Chinese president Xi Jinping, aimed to build a trade and infrastructure network that would connect Asia with Europe and Africa along the land-based Silk Road Economic Belt and the ocean-based Maritime Silk Road. More than 100 countries and international organizations are or will be involved in this program, which will affect nearly two-thirds of the global population and approximately a quarter of all goods and services needed for global functioning [163]. Undoubtedly, however, this program will present new challenges to Chinese parasitic disease control programs. The detection of imported cases and the provision of prompt treatment will be essential to reducing the risk of an outbreak of parasitic disease, particularly of nonindigenous parasites, as the establishment of a new parasite may lead to catastrophic consequences. Therefore, universal participation in the campaign against imported parasitic diseases in mainland China is required and includes the transmission of information regarding health care organizations (clinics and hospitals), disease control and prevention centers (CDC), governmental public health departments, entry and exit administrations, labour service companies, transnational corporations, and tourist administrations.

Strengthening the essentiality of professional education and updated training for medical care personnel

The parasitic disease control program in China has made impressive progress, and its status is particularly important, particularly with regard to the rapidly developing economy in mainland China. This program is especially essential to highly developed areas such as Guangdong, Shanghai, and Beijing, where fewer resources are available to communicate knowledge about parasitic diseases [162]. In the absence of sufficient financial resources, general practitioners and specialists might no longer be equipped with sufficient parasitological knowledge. Accordingly, primary health care providers might misdiagnose many cases of malaria as a cold or flu, leading to delayed treatment [26, 45, 64, 70, 79, 81]. As a result, some patients might not receive an accurate diagnosis even after referral to a specialist [57, 63, 68, 71], and the resulting treatment delay may be lethal for patients infected with P. falciparum.

Furthermore, technicians may not be able to differentiate Plasmodium species in blood smears [26, 34, 42, 94, 105], especially in small hospitals without DNA detection-related equipment, and patients with P. falciparum co-infection have died after receiving a diagnosis of the less-serious P. vivax malaria [20, 105]. A recent report describes the case of a 36-year-old male migrant worker who was misdiagnosed with a ureteral calculus, invasive urothelial carcinoma, and eosinophilic cystitis at several hospitals after returning from Angola. The patient underwent several treatments, including transurethral bladder tumor resection, before finally receiving a definite diagnosis of schistosomiasis haematobia after a pathology examination revealed eggs in the bladder tissue [146]. The eventual diagnosis occurred one year after his first visit to the clinic, and his subsequent experience had both physical and mental effects. Similarly, more than two months were required to receive a final diagnosis in the first case of human African trypanosomiasis in China. During this delay, the trypanosome parasites were able to cross the blood-brain barrier and enter the spinal fluid to infect the central nervous system, leading to irreversible damage [159]. Although imported cases are difficult to diagnose, much can be done to avoid future tragedies. Among medical care personnel, the awareness of parasitic diseases and parasitological knowledge must be improved. Professional parasitological education should be strengthened, rather than neglected, in medical schools. Furthermore, regular training courses are needed to ensure that relevant medical personnel receive updated knowledge and improve their expertise.

Putting Chinese migrant workers as a priority group for health education and public awareness of imported diseases

As mentioned above, the number of Chinese migrant workers is expected to increase rapidly to meet the goals of large Chinese governmental programs such as “Aid to Africa” and the Belt and Road Initiative. Most migrant workers will participate in outdoor work projects, including the construction of water reservoirs, electric power stations, and roads and in mining and oil exploitation. These workers tend to have a lower socioeconomic status and education level and are thus less likely to possess adequate health knowledge. Accordingly, they are vulnerable to environmental risk factors such as contact with unsafe water and insect bites and are therefore very susceptible to parasitic infection. Therefore, labour service companies must conduct health education activities, distribute medicine, and provide necessary personal protective equipment to the migrant workers before they leave China. Governmental health departments should also provide guidance and supervision during this process. In practice, however, these procedures fall short of the targets. Some returnees understand that they might have developed malaria if they have a fever, and this knowledge can help the physician make a timely diagnosis [81]. More commonly, however, the returnee does not know what type of disease he or she might have acquired, and the connection between the disease and health risk behaviour remains hidden. Furthermore, some returnees do not report their travel history to the physician, which contributes significantly to misdiagnosis [75, 101]. Accordingly, more resources should be allocated to the health education of prospective migrant workers. For example, CDCs could assign professionals to deliver informative lectures to those workers. Other people, such as businessmen, students, technicians, and travelers, are also susceptible to parasitic infection. Therefore, information departments and tourist administrations should also raise awareness of the potential dangers by distributing brochures, displaying posters, and playing promotional videos.

Intensifying the management and surveillance of people entering China (international and domestic passengers)

Imported parasitic diseases are an inevitable and increasingly common consequence of globalization, as well as international and regional communications and cooperation. Issues related to the management and surveillance of people entering China are broad, high-level, and cross-cutting. Travel between different environments will inevitably result in the importation of parasitic disease agents and the introduction of new parasites to China. In the absence of a sound management and surveillance system, such travel might lead to the formation of an endemic focus, especially if the parasite vector (snail, mosquito) is present in China.

The number of domestic travellers continues to grow steadily, as demonstrated by the increasing number of Chinese travellers to other countries (101, 117, and 122 million person-times in 2014, 2015, and 2016, respectively) [164166]. The number of international visitors (and compatriots from Hong Kong, Macao, and Taiwan Province) has also increased (128, 134, and 138 million persons in 2014, 2015, and 2016, respectively) [164166]. While traveling, domestic passengers might acquire certain infections because of a lack of knowledge about transmission and a lack of specific antibodies. These factors are especially important for travelers who visit Africa and Southeast Asia and for international visitors from endemic areas who may have already developed or will develop the disease. Thus, entry inspection plays a vital role in the management of such potential infection sources. The CDC staff should monitor the health service usage and health outcomes of suspected or confirmed cases of a certain parasitic diseases. For example, the condition of a 43-year-old migrant worker with falciparum malaria worsened after a failure to comply with medical instructions provided by the CDC staff [44]. The development of management and surveillance guidelines, particularly for non-endemic parasitic diseases, is increasing in importance.

Increasing investigation of the distribution of introduced/potential vectors and susceptibility to parasites

The Chinese population is increasingly at risk of contracting parasitic diseases that are not indigenous to China as a result of the return of infected travelers or the arrival of infected foreigners [167, 168]. The risk of transmission of such diseases increases when the parasite vectors are present in or have been introduced to China. The natural S. mansoni vector, Biomphalaria straminea, was found in Hong Kong in 1974. In 2013, its distribution was found to have expanded to nearby cities such as Shenzhen, Dongguan, and Huizhou, Guangdong, and it might since have spread via waterways in Guangdong [7]. Because the Guangdong region is characterized by many rivers and frequent international communications, the parasite’s life cycle may be established by the introduction of patient fecal matter into water containing Biomphalaria snails. This would be a matter of great public concern. For other nonindigenous parasitic diseases such as Chagas disease (Trypanosoma cruzi), the vector (triatomine insects) was found to be distributed throughout China [169], although the susceptibility of the vector to T. cruzi remains unclear. Therefore, it is important to understand both the distribution of the vectors and their susceptibilities to parasites. The CDC staff and scientific researchers should collaborate to conduct relevant field investigations and laboratory research.

Improving diagnostic techniques and drug stocks

Many parasitic diseases are clinically curable if treatment is initiated at an early stage. Therefore, universal access to rapid diagnosis and care is essential. However, the diagnosis of an imported parasitic disease is complex and requires specialized staff, because many diagnostic techniques are far from satisfactory. For example, the current rapid diagnostic tests for malaria are somewhat unreliable, and repeated false-negative cases [46, 61, 86] have led to multiple missed diagnoses at ports of entry and community health care centres. Although the microscopic examination of a peripheral blood smear is currently the gold standard for malaria diagnosis, this technique is limited by a high false-negative rate [41, 84], especially in cases with low degrees of parasitemia. Furthermore, it is difficult to differentiate among Plasmodium species, and coinfections are often missed [27]. Although DNA detection techniques have been developed to overcome these limitations [21], these methods are much more expensive, and each small clinic cannot realistically be supplied with an expensive PCR amplifier and skilled technicians. Accordingly, early, rapid, economically feasible, and accurate diagnostic methods are in desperate demand. Foundations should support studies in this field and encourage researchers to conduct related studies. In addition, because the rapid diagnosis of an imported parasitic disease is meaningless without prompt treatment, access to therapeutic interventions for rare parasitic diseases is also a significant factor. The CDC should establish a secure drug supply system to guarantee that patients with rare infections can obtain timely therapeutic interventions.

Conclusions

In the context of globalization, which is underscored by large Chinese governmental programs such as “Aid to Africa” and the “Belt and Road Initiative”, the Chinese parasitic disease control program will face new challenges. For example, imported cases of disease represent a major obstacle to the elimination of several parasitoses such as malaria and schistosomiasis, and some nonindigenous pathogens (and their vectors) have emerged in mainland China. Therefore, China should act to meet these challenges, which are closely associated with national biological safety.

Abbreviations

CDC: 

Centers for Disease Control and Prevention

Declarations

Acknowledgements

We thank Professor Heinz Mehlhorn (Heinrich Heine University, Germany) and Professor Moussa Sacko (Ministry of Health, Mali) for providing helpful comments and suggestions.

Funding

This work was supported by grants from the National Key R&D Program of China (No. 2016YFC1200500), the National Natural Science Foundation of China (No. 81601781) and the China Postdoctoral Science Foundation (No. KLF201012).

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author upon reasonable request.

Authors’ contributions

ZD-W directed and coordinated the study. LG-S and XD-Z were responsible for the literature review. LG-S analysed the data, drew the images and wrote the first draft. XD-Z, YX-L, BB-Z, XY-W, DJ-Y and ZD-Wu revised the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510080, Guangdong, China
(2)
Key Laboratory of Tropical Diseases Control (SYSU), Ministry of Education, Guangzhou, 510080, Guangdong, China
(3)
Provincial Engineering Technology Research Center for Biological Vector Control, Guangzhou, 510080, Guangdong, China
(4)
Jiangxi Provincial Testing Center of Medical Apparatus and Instruments, Nanchang, 330029, Jiangxi, China
(5)
School of Public Health, Fudan University, Shanghai, 200433, China

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