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    Cumulative cases and distribution of strongyloidiasis in China, 1973–2011. GD, Guangdong Province; GX, Guangxi Province; TW, Taiwan Province; FJ, Fujian Province; HK, Hong Kong; HN, Hainan Province; ZJ, Zhejiang Province; JS, Jiangsu Province; HB, Hebei Province; AH, Anhui Province; HN1, Hainan Province; YN, Yunnan Province; JX, Jiangxi Province; HB1, Hubei Province; HN2, Henan Province; SC, Sichuan Province; NM, Neimeng Province.

  • View in gallery

    Annual number of strongyloidiasis cases in China, 1973–2011.

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    Occupation distribution of patients with strongyloidiasis in China, 1973–2011.

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    Age distribution of patients with strongyloidiasis in China, 1973–2011.

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    Symptoms and other diseases among patients with strongyloidiasis in China, 1972–2011. EOS = eosinophils.

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Strongyloidiasis: An Emerging Infectious Disease in China

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  • Key Laboratory of Prevention and Control for Emerging Infectious Diseases of Guangdong Higher Institutes, School of Public Health and Tropical Medicine, Southern Medical University, Guangzhou, Guangdong, China; Department of Traditional Chinese Medicine, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong, China; Program in Public Health, and Departments of Microbiology and Molecular Genetics and Molecular Biology and Biochemistry, University of California, Irvine, California

Since the first case of strongyloidiasis reported in China in 1973, there have been 330 confirmed cases as of 2011. The present study conducted a meta-analysis on 106 cases for which detailed information on clinical symptoms, diagnosis, and outcome was available. Most (63%) cases were from the past decade. Immunocompromised patients and those given cortical hormones accounted for 68% of the cases, and case-fatality rate was 38%. General clinical symptoms included abdominal pain (53%), diarrhea (46%), fever (40%), and vomiting (39%). The parasite positivity rate in feces, sputum, and urine by microscopic diagnosis was 75%, 24%, and 8%, respectively, and gastrointestinal endoscopy or other biopsy detection rates were 17%. A lack of specific clinical manifestations makes early diagnosis and correct treatment difficult. Strongyloidiasis is an emerging disease in China, and public and clinical awareness needs to be raised to improve prevention and control.

Introduction

Strongyloides stercoralis (Bavay, 1876) was first described in Vietnam from a fecal sample of a French soldier with diarrhea. It is a facultative pathogen, alternating opportunistically between a free-living and parasitic life cycle. Adult worms reside in the intestine during the parasitic cycle, and larvae may invade the lungs, brain, liver, kidney, and other organs, resulting in strongyloidiasis.1 The incidence of strongyloidiasis is increasing in many developing countries and is facilitated by international travel and immigration,2,3 and increasing numbers of immunosuppressed or immunocompromised patients. Misdiagnosis and missed diagnosis resulting from the lack of disease-specific manifestations contribute to it being a neglected tropical disease.4

We reviewed and analyzed strongyloidiasis cases reported in China.598 The first documented patient was from Guangxi Province in 1973. Since that time, 330 cases have been reported. We focus on 106 cases for which detailed information, including analysis of clinical symptoms, diagnosis, treatment, and epidemic distribution, is available. We expect that this analysis will highlight the importance of strongyloidiasis in China, enhance clinical diagnostic ability, and arouse public attention to prevention.

Methods

Strongyloides stercoralis was used as key word to search all relevant articles in the China National Knowledge Infrastructure database, the VIP Database for Chinese Technical Periodicals, the Wanfang database, as well as PubMed, ScienceDirect, and Springerlink. Publications related to strongyloidiasis reports in China were reviewed and characterized for parasitology, epidemiology, symptom and signs, diagnosis, treatment, and prevention.

Results and Discussion

Parasitology.

Free-living, infective S. stercoralis filariform larvae can penetrate the skin and initiate the parasitic life cycle, a mode of transmission similar to hookworm.1 The larvae migrate to the digestive system via the circulatory system and invade and colonize the small intestinal (mostly duodenal and jejunal) mucosa, where they develop into adult worms. Adult female worms usually reside under the intestinal mucosa where they shed eggs. Fertilized eggs produce rhabditiform larvae that exit the mucosa into the intestinal cavity from which they are excreted in the feces. The parasitic life cycle likely includes autoinfection, especially in immunosuppressed or immunocompromised hosts. Three routes are possible: direct endo-autoinfection during which rhabditiform larvae hatch and continue to develop in the mucosa and circulate to other organs and tissues via the circulatory system; indirect endo-autoinfection characterized by rhabditiform larvae escaping the mucosa and developing into filariform larvae in the intestinal cavity and invading the circulatory system from the colonic mucosa or lower intestine; and exo-autoinfection whereby filariform larvae excreted from the feces re-infect the host from perianal skin.

Epidemiology.

Thirty to 100 million persons worldwide are infected with S. stercoralis, and most cases are in tropical, subtropical, and temperate regions.4 The National Human Parasite Distribution survey has reported strongyloidiasis in 26 Provinces (cities and districts) in China, mainly in the southern regions of this country (Figure 1). Prevalence countrywide averages 0.12%, and some regions have rates as high as 11.0–14.0%.1 The farming areas of Tianyang and Baise Counties (Guangxi Province) had an average infection rate of 3.69%.99 Residents of Qiaozhuang, Boxing County (Shandong Province), had an S. stercoralis infection rate of 1.29% (11 of 854), with no obvious differences in sex and age distribution.100 A survey in Menghai County (Yunnan Province) reported an infection rate of 11.6% (29 of 250).101

Figure 1.
Figure 1.

Cumulative cases and distribution of strongyloidiasis in China, 1973–2011. GD, Guangdong Province; GX, Guangxi Province; TW, Taiwan Province; FJ, Fujian Province; HK, Hong Kong; HN, Hainan Province; ZJ, Zhejiang Province; JS, Jiangsu Province; HB, Hebei Province; AH, Anhui Province; HN1, Hainan Province; YN, Yunnan Province; JX, Jiangxi Province; HB1, Hubei Province; HN2, Henan Province; SC, Sichuan Province; NM, Neimeng Province.

Citation: The American Society of Tropical Medicine and Hygiene 88, 3; 10.4269/ajtmh.12-0596

Ninety-four reports of strongyloidiasis were reported during 1973–2012, and 106 cases in these reports are accompanied by detailed information. After the described case in 1973, an additional four cases were documented in the subsequent decade (1973–1982). Case reports have increased every year since 1985, except in 1992 and 1997, and 58% of the 106 cases occurred during the past 10 years (2002–2011) (Figure 2). Case reports were from provinces and autonomous regions, most of which are south of the Yangtze River. A total of 21% (22 of 106), 13% (14 of 106), and 11% (12 of 81) of the cases originated in Guangdong, Guangxi and Taiwan, respectively (Figure 1). Small geographic clusters of cases were evident in Lufeng, Guangdong (four cases);11,64 Nanping, Fujian (three cases);30,35,43 and Yunxiao County, Fujian (two cases).65,67 Clustering also was evident in families in rural areas.64

Figure 2.
Figure 2.

Annual number of strongyloidiasis cases in China, 1973–2011.

Citation: The American Society of Tropical Medicine and Hygiene 88, 3; 10.4269/ajtmh.12-0596

One-hundred and three of the 106 cases reported sexes of the patients (71 male patients and 32 female patients) (male:female ratio = 2.19:1). A total of 54 reports documented occupation; 64% described as peasants, workers (15%), or students (9%) (Figure 3). Some patients in the worker groups worked on farms,33,65,67 and most of the student patients lived or came from villages.64,86 This distribution and sex ratio bias (males are the principal field workers) support the conclusion that rural populations have the highest risk for strongyloidiasis. This risk probably results the agrarian living and working environment and frequent exposure to soil. The age distribution of the 91 patients for which records are available are consistent with increased exposure with age. Although the youngest and oldest patients were 5 and 88 years of age, respectively,17,55 69% of the patients were > 41 years of age, and persons 41–50 years of age accounted for the largest number of cases (25) (Figure 4).

Figure 3.
Figure 3.

Occupation distribution of patients with strongyloidiasis in China, 1973–2011.

Citation: The American Society of Tropical Medicine and Hygiene 88, 3; 10.4269/ajtmh.12-0596

Figure 4.
Figure 4.

Age distribution of patients with strongyloidiasis in China, 1973–2011.

Citation: The American Society of Tropical Medicine and Hygiene 88, 3; 10.4269/ajtmh.12-0596

Clinical features.

Larval and adult S. stercoralis are pathogenic, and severity of diseases is correlated closely with worm burden (intensity of infection) and immunologic status of the host. People with normal immune system function generally will not have clinical symptoms if infected mildly (low worm burden). A chronic autoinfection may persist for several years with occasional gastrointestinal symptoms. In contrast, immunecompromised patients may have disseminated hyperinfection characterized by mass migration of the larvae inside the body. Invasion of the brain, liver, lung, and kidney results in severe damage that can progress to organ failure and death.

Strongyloidiasis patients have mainly non-specific gastrointestinal symptoms, including nausea, vomiting, abdominal pain, diarrhea accompanied by fever, anemia, and malaise. General clinical symptoms in the 106 detailed reports included abdominal pain (53%), diarrhea (46%), fever (40%), vomiting (39%), and lack of appetite (24%) (Figure 5). Severe infection can be complicated with gastrointestinal bleeding, leading to hemorrhagic anemia, kidney failure, and death.20 Patients with massive gastrointestinal infection may have intestinal obstruction.6,10,32,64

Figure 5.
Figure 5.

Symptoms and other diseases among patients with strongyloidiasis in China, 1972–2011. EOS = eosinophils.

Citation: The American Society of Tropical Medicine and Hygiene 88, 3; 10.4269/ajtmh.12-0596

Strongyloidiasis patients may also have stiff necks and severe headaches as a result of infection of the brain. One case diagnosed as intracranial strongyloidiasis was confirmed by magnetic resonance imaging.28 The patient ceased therapy and returned home for economic reasons. The patient's condition worsened and resulted ultimately in systemic failure and death. Filariform larvae were detected in the cerebrospinal fluid of another patient but this person recovered fully after a course of treatment.44 Other reported cases of strongyloidiasis involve the urinary system; one patient had frequent, urgent, and painful urination but no diarrhea history, and a six-year-old patient infected in the spine had dyskinesia of both lower limbs.14,36

Eosinophil data were available for 55 of the 106 cases; 35 increased (63%), 8 were normal (15%), and 12 decreased (22%). The highest eosinophil value reported was 38.4% (absolute value of 4.81 × 109 cells/L), and the lowest value was 0%.7,46,47,67,81,88 Helminth infections are accompanied by elevated levels of eosinophis. However, this finding may occur with S. stercoralis infections. More research is needed to determine whether the relationship of eosinophils with these infections.

Strongyloides stercoralis infection may lead to elevated IgE levels in patients. There were only 12 documented immunity test reports among our samples, and these include 5 reports with IgE levels three-fold higher than the reference range (< 200 IU/mL or < 0.009 g/L).15 Among the five case-patients, one patient with an IgE level of 638.53 IU/mL had a severe infection and eventually died.47 There were two case-patients with pulmonary disseminate infections and IgE levels of 736 IU/mL and 739 IU/mL.13,17 Two other patients had mild infections and IgE levels of 2,560 IU/mL and 2.09 g/L.23,83 The IgE values increased in all five patients, and changes in range were generally inversely proportional to the degree of infection. Patients with mild infections had the most significant increase in IgE levels. Patients with severe or disseminated infections had relatively lower levels of IgE.

Seventy-two (68%) of the 106 strongyloidiasis patients had other diseases, including rheumatoid arthritis, systemic lupus erythematosus, diabetes, nephrotic syndrome, chronic obstructive pulmonary disease, and carcinoma, or used immunosuppressive drugs (Table 1). All of these patients were expected to have suppressed immunity that exacerbates a disseminated infection and results in severe symptoms and death. The mortality rate of the 72 patients was 37.5% (27 of 72). Disseminated strongyloidiasis occurs usually among immunosuppressed patients, such as those with malignant tumors or those using immunosuppressive agents (especially steroids). However, patients with acquired immunodeficiency syndrome did not show many disseminated infections and the reasons for this are unclear. One possible explanation is that the level of CD4+ cells had not decreased much when patients with acquired immunodeficient syndrome died.102 Patients with diabetes and nephrotic syndrome have higher disseminated strongyloidiasis infection rates. Diabetes patients may prevent severe strongyloidiasis infection through immunologic screening.102,103

Table 1

Underlying characteristics associated with human strongyloidiasis in China, 1973–2011

CharacteristicNo. cases
Carcinoma7
Rheumatoid arthritis7
Systemic lupus erythematosus5
Chronic obstructive pulmonary disease6
Nephrotic syndrome7
Diabetes5
Allergic purpura3
Chronic bronchitis2
Rheumatic heart disease2
Fisher syndrome1
Sjogren's syndrome1
Scleroderma1
Endobronchial tuberculosis1
Meningitis1
Duodenal ulcer1
Induction of labor1
Parasitosis9
Drug abuse1
Steroid therapy for other diseases10

Diagnosis and treatment.

The lack of specific clinical features resulting from S. stercoralis infection results in a high percentage of misdiagnosed cases. Twenty-three of the 106 cases were diagnosed initially as ancylostomiasis (6 cases), carcinoma (2 cases), gastritis (3 cases), enteritis (3 cases), bronchitis (1 case), and dysentery (1 case) before follow-up examinations confirmed strongyloidiasis. Therefore, strongyloidiasis should be considered and ruled out for all immunocompromised patients from high-risk regions (rural) who have gastrointestinal and respiratory symptoms. Patients with bloody, purulent, or watery feces should be tested to differentiate strongyloidiasis from shigellosis or amebic dysentery.54,69 Similarly, patients with abdominal pain should be examined to differentiate strongyloidiasis from gastritis and duodenitis.26,33,37

Diagnosis of strongyloidiasis is based mainly on detection of rhabditiform or filariform larvae in samples of feces, sputum, gastric juices, and cerebrospinal fluid. Immunologic techniques, such as enzyme-linked immunosorbent assay and immunoblots, and molecular methods based on gene amplification can also be useful in diagnosis.104 Seventy-five percent of the 106 patients tested positive in stool specimens, while 24, 8, 4 and 2% were positive in sputum, urine, vomit and duodenal drainage specimens, respectively. Approximately 1% of the patients had positive results for strongyloidiasis in gastric juices, hydrocele, cerebrospinal fluid, scrotal hydrocele fluid, and pericardial effusions. Gastrointestinal endoscopic biopsy and other pathologic examination detected 17% of the cases, and fiber optic bronchoscopy accounted for an additional 1%. Twenty-nine percent of the patients tested were pathogen positive for more than one specimen.

Strongyloides stercoralis of every developmental stage were detected among the 106 cases (Table 2). Rhabditiform and filariform larvae were reported in 48% and 20% of the cases, respectively, and 14% had eggs. Male and female adult worms were detected simultaneously in stool specimens in two cases. Male worms are seldom seen in human host,71,82 and there is debate as to whether they are part of the parasitic life cycle. However, there are a number of early reports of males in diseased patients.105

Table 2

Diagnosis of human strongyloidiasis in China, 1972–2011*

SampleNo. casesDevelopmental stage
RLFLEggAdult (female)Adult (male)
Feces704411932
Sputum18114110
Urine981200
Vomit431200
Gastric juices100110
Cerebrospinal fluid101000
Hydrocele101000
Duodenal drainage100100
Gastric/duodenal biopsy1821520
Fiber optic bronchoscopy100100

From 106 cases described in the text. RL = rhabditiform larvae; FL = filariform larvae.

Treatment.

Treatment of strongyloidiasis should begin after diagnosis and apply the principles of early treatment with sufficient dosage and duration to cause complete worm elimination. Traditionally, tiabendazole is the drug of first choice with other options including mebendazole, albendazole, and levamisole. Seventy-nine of the 106 case reports contained detailed information on drug treatments and albendazole was the choice for 62% (49 of 79) of the patients with dosage provided based on the patient's condition. Regimens of 400–800 mg, twice a day for 3–10 days, resulted in a cure rate of 61%. Patients with obstinate strongyloidiasis or albendazole resistance can be treated with ivermectin54 and 3 of 106 patients receiving this drug recovered fully.17,31 Traditional Chinese medicine also was effective; three cases of strongyloidiasis accompanied by allergic purpura were cured after oral administration of 10 g of guan zhong, three times a day for seven days, then a 7–10 days break, followed by another course for one week.41 Gentian violet was recommended for three patients with renal failure. One case of strongyloidiasis accompanied by hemorrhagic enteritis was treated with 90 mg/day of gentian violet for 14 days and the patient recovered and was discharged.78

Prevention.

The incidence of strongyloidiasis in China has been increasing in recent years, especially in the southern region, and rural and immunocompromised populations at highest risk. Because the disease has nonspecific clinical features, it is easily to misdiagnosis. Medical professionals, especially doctors and diagnosticians, should improve their diagnostic and differential diagnostic capabilities. High-risk population should be made aware of the infection threat and instructed in preventative measures. Patients receiving immunosuppressive therapy who have gastrointestinal symptoms should be tested to exclude strongyloidiasis.

Recommendations for prevention of strongyloidiasis in China include not being barefoot while working or traveling in fields in strongyloidiasis-epidemic regions. Raw vegetables and fruits should be washed multiple times with clean fresh water to avoid possible S. stercoralis contamination. Patients with immunocompromised or immunosuppressed conditions or those initiating immunosuppressive therapy should be screened for S. stercoralis infection. Persons with positive test results should be treated before onset of symptoms or with the other proposed therapies. Patients receiving steroid hormones (dexamethasone) for long periods should take preventative medications (albendazole) for strongyloidiasis every three months.

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Author Notes

* Address correspondence to Xiaoguang Chen, Key Laboratory of Prevention and Control for Emerging Infectious Diseases of Guangdong Higher Institutes, School of Public Health and Tropical Medicine, Southern Medical University, Guangzhou, Guangdong, 510515, China. E-mail: xgchen2001@hotmail.com

Financial support: This study was supported by grants from the National Natural Science Foundation of China (U0832004) and Guangdong University of Foreign Studies GDUPS (2009) to Xiaoguang Chen.

Authors' addresses: Chunmei Wang, Jiabao Xu, and Xiaohong Zhou, Department of Parasitology, Southern Medical University, Guangzhou, China, E-mails: wangcmq@163.com, xujiabao007@gmail.com, and daizhouxh@163.com. Juan Li, Nanfang Hospital, Southern Medical University, Gaungzhou, China, E-mail: lj40038@126.com. Guiyun Yan, Program in Public Health, University of California, Irvine, CA, E-mail: guiyuny@uci.edu. Anthony A. James, Department of Molecular Biology and Biochemistry, University of California, Irvine, CA, E-mail: aajames@uci.edu. Xiaoguang Chen, No 1023 Shatai South Road, Guangzhou, China, E-mail: xgchen2001@hotmail.com.

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