Journal List > J Korean Med Sci > v.33(44) > 1107923

Kim, Ahn, Sohn, Nawa, and Kong: Human Sparganosis in Korea

Abstract

Background

Sparganosis is a larval cestodiasis caused by the plerocercoid of Spirometra spp. Since the first description of human sparganosis in 1924, several hundred cases have been reported in Korea. However, systematic approaches for literature surveys of Korean sparganosis have seldom appeared.

Methods

We searched publicly available databases such as PubMed, Research Information Sharing Service, and Korea Medical Citation Index with relevant Medical Subject Headings.

Results

At least 438 Korean sparganosis cases have been described from 1924 to 2015. Preoperative diagnosis has been significantly increased since the 1980s due to popularization of serological and imaging diagnostics. Cases were largely detected from fifth decades in general, but cerebral sparganosis was detected in relatively young age groups (third and fourth decades). Sparganosis was prevalent in men (75.9%). Consumption of frog/snake and drinking unfiltered water were found in 63.4% and 16.9% of patients, respectively. Most frequently affected sites were subcutaneous tissues (49.9%), followed by the central nervous system (36.2%). Involvements of visceral organs (7.6%), ocular regions (3.6%), and muscles (2.7%) were noticed. In women, breast sparganosis constituted a large proportion (34.2%). Sparganosis associated with immunocompromised patients has recently been reported.

Conclusion

Sparganosis has been continuously reported in Korea during the past 90 years, although its incidence has decreased during the last 20 years. The disease is mostly characterized by subcutaneous nodule, but infection of the worm in vital organs often results in serious illness. Continuous awareness is warranted to monitor sparganosis occurrence and associated clinical consequences.

Graphical Abstract

jkms-33-e273-abf001.jpg

INTRODUCTION

Sparganosis is a larval cestodiasis (metacestodiasis) triggered by infection with the plerocercoid of Spirometra spp. of which adults thrive in the small intestine of canine or feline host (https://www.cdc.gov/dpdx/sparganosis/index.html). Humans mostly serve as an intermediate host and are infected with larval worms (plerocercoid: sparganum, pl. spargana). The sparganum might grow into an adult in human intestine in extremely rare cases.1 Drinking unfiltered water that contains cyclops infected with procercoid and/or ingesting raw or inadequately cooked flesh of frogs/snakes or other paratenic hosts are important sources of human infections. Application of raw flesh/skin of poikilothermic intermediate hosts to subside sore edema and ophthalmitis is also a risk factor.234
Sparganosis has been sporadically detected globally, but the majority of cases occurred in East and Southeast Asian countries in relation to their eating habits and traditional medical practice.4 The disease is principally characterized by a slowly migrating subcutaneous nodule(s), but infection may occur in any part of the body. Infection of the worm(s) in vital organs often results in serious illness. The parasite might invoke symptoms as early as two months postinfection.2 Sometimes patients could remain asymptomatic for approximately 17 years.3 Different Spirometra spp. can cause human infections. Spirometra mansoni in Europe, Spirometra mansonoides in America, and Spirometra erinaceieuropaei in Asia including Korea.5 A recent morphological and molecular study has demonstrated that Spirometra decipiens plerocercoid is involved in Korean sparganosis.6
Sparganosis has not been uncommon in Korea. The following factors might be associated with the development of disease. Farmers working in rice paddies or in the forest might drink unfiltered water when they are thirsty during work as a long traditional lifestyle of aquaculture or forestry activity. Some people used to consume flesh of frog and/or snake to treat tuberculosis, arthralgia, and neuralgia.3 Previous seroepidemiological surveys of apparently healthy persons in Korea have demonstrated seropositive rates of 1.7%–3.3% for sparganosis. Large proportions (40.4%–62.5%) of seropositive people were old men aged over sixth decades,78 suggesting that such traditional habits might be linked to hidden infections, although non-specific serological cross-reactions by some other underlying factors could not be ruled out.9
In Korea, an authentic case of sparganosis in the lower leg was firstly found in 1917 which was described in 1924.10 Several hundreds of cases were thenceforward reported. However, systematic approaches of literature survey of human sparganosis in Korea have rarely appeared.2311 In the present study, we provide an overview and perspectives of human sparganosis in Korea by mining the publicly available databases during the period of 1924 to 2015.

METHODS

Literature survey

Published reports were searched from publicly available databases which included PubMed (www.ncbi.nlm.nih.gov/pubmed), Research Information Sharing Service (RISS; https://www.riss.kr), and Korea Medical Citation Index (KoMCI; https://komci.org/). We used terms “sparganosis,” “Spirometra,” and “Korea” in conjunction with associated Medical Subject Headings (MeSH) in the National Library of Medicine (https://www.nlm.nih.gov/mesh/).

Collection of sparganum from Korean terrestrial snakes

We examined 81 terrestrial snakes that had been caught in the southern part of Korea (Gyeongsangnam-do). Those snakes were donated by the Association of Wild Animals Protection for research purpose, including 38 Agkistrodon brevicaudus, 25 Rhabdophis tigrinus, and 15 Elaphe rufodorsata. The snakes were individually anesthetized with ethyl ether and sacrificed. Each snake was examined for the presence of sparganum.

Ethics statement

Euthanasia of moribund snakes was approved by the Institutional Review Board of Gyeongsang National University School of Medicine (approval No. GNU-03-008). Informed consent was not needed.

RESULTS

Survey of Korean sparganosis cases in publicly available domains

We were able to collect information on 438 human sparganosis cases from 159 articles published in 51 journals. We found 55 papers in PubMed and 104 papers in two Korean paper search sites (RISS and KoMCI). Twenty-six and 75 articles were independently listed in PubMed and Korean search sites, respectively, among which 29 articles could be found in all search conditions. Out of the 51 Journals, the largest number of articles dealt with human sparganosis had been found in the Korean Journal of Parasitology, which contained 156 case reports. A total of 48 cases of human sparganosis were reported in the Journal of the Korean Society of Radiology. In addition, 35 and 12 cases were retrieved from the Journal of Korean Neurosurgical Society and the Korean Journal of Urology, respectively. The other 187 cases were reported in Radiology, Neuroradiology, Urology, and other international journals (We only listed three major journals that published the most Korean sparganosis).

Epidemiological characteristics

We analyzed the number of sparganosis cases reported in Korea during the period of 1924 to 2015 (Fig. 1). A previous study reported a total of 63 cases during the period of 1924–1974: 58 cases from 1924 to 1973 and additional five cases in 1975.3 At that time, preoperative diagnosis of sparganosis was almost impossible. Moreover, academic capacity to preserve medical literature between 1944 and 1953 had been chaos due to social crisis. Social and medical infrastructures were very poor in Korea, which might have hampered appropriate evaluation of medical situations including those of sparganosis.23
Fig. 1

Decennial distribution patterns of human sparganosis reported in Korea during 1924–2015. At least 438 sparganosis cases were reported in Korea. Cases reported between 1924 and 1953 referred to cases recorded in Korean peninsula and those after 1954 represented sparganosis reported in the Republic of Korea. Duplicated publications were excluded by reviewing individual papers.

aMost medical records in Korea were not preserved during 1944–1953 due to the Pacific War (1941–1945), post-war chaos (1945–1948) and the Korean War (1950–1953).3
jkms-33-e273-g001
Since the late 1970s, human sparganosis continue to occur in Korea. Min11 found additional 56 cases through literature survey between 1975 and 1989. Our literature search revealed that a total of 243 cases were described between 1984 and 2003 (Fig. 1) including those listed by Cho et al.3 and Min.11 Thereafter, cases seemed to be decreased to some extent. Nevertheless, sparganosis cases have been continually reported during the last 15 years (94 cases between 2004 and 2015).
A drastic increase of sparganosis cases from the early 1980s might be due to the development and popularization of diagnostic modalities which allow easier and earlier detection of preoperative patients. Imaging diagnostics including computed tomography (CT)/magnetic resonance imaging (MRI)/ultrasonography (US) have become widely applied for the diagnosis of sparganosis, through which pathognomonic signs for sparganosis are established (see also later sections).1213 Serological tests using crude extracts of the sparganum as antigen has yielded sensitivity of 85.7%–90% and specificity of 87%–97.5% and purified protein fractions of 31 and 36 kDa have exhibited sensitivity and specificity over 95%.91415 By these means, preoperative diagnosis of sparganosis cases, especially those of the central nervous system (CNS) and subcutaneous tissues including breast, has been substantially improved.
Fig. 2 shows age and gender distribution of patients. Patients were largely diagnosed between their third and sixth decades. However, 10 cases (2.5%) were detected in their early ages (under 10 years), suggesting that people might have been exposed to infection sources from childhood. Among cases with available demographic data (398 cases), the incidence of sparganosis was 2.5 times higher in men (284 cases) than that in women (114 patients).
Fig. 2

Age and sex distribution of sparganosis cases in Korea. Among 438 cases, 284 patients were men and 114 patients were women. We could not trace personal information for 40 cases.

jkms-33-e273-g002
Drinking unfiltered water contaminated with cyclops harboring procercoid and/or contraction with snakes/frogs infected with plerocercoid might be intimately involved in human sparganosis.23 We analyzed such behavioral habits of patients. Ingestion of snake and/or frog was recognized in 63.4% (203 patients) of patients whose eating history was available (320 cases). Drinking unfiltered water was also observed in 16.9% (54 cases) of these patients. However, 19.7% (63 cases) of patients denied exposure to any possible infection source (Table 1).
Table 1

Behavioral habits of Korean sparganosis casesa

jkms-33-e273-i001
Sources No. of cases (%)
Snakes and frogs 63 (19.7)
Snakes 101 (31.6)
Frogs 39 (12.2)
Unfiltered water 54 (16.9)
Negative 63 (19.7)
Subtotal 320 (100.0)
Not-available 118
Total 438
aConsumption and drinking experiences of intermediate/transport hosts related to transmission of sparganosis.
Many studies have observed infection status of the sparganum in frogs and snakes in Korea from the mid-1920s to the mid-1980s.11161718 Examination of snakes and frogs revealed variable infection rates of 3.1%–100%. Infection status of snakes was higher than that of frogs.11 In 2003, we examined 81 Korean terrestrial snakes including 38 Agkistrodon brevicaudus, 25 Rhabdophis tigrinus and 15 Elaphe rufodorsata with an aid from the Association of Wild Animals Protection because those snakes were illegally caught. We observed that the infection rate reached 60.5%–92.5%, with mean worm density of 37.7 worms per snake (Table 2). This result confirmed that snakes might be an important intermediate/paratenic host related to transmission of sparganosis to humans.
Table 2

Infection status of sparganum in terrestrial snakes collected from Gyeongsangnam-do, Korea (2003)

jkms-33-e273-i002
Species of snake No. of examined No. of infected (%) No. of spargana detected
Total Range Average
Agkistrodon brevicaudus 38 23 (60.5) 355 1–215 15.4
Rhabdophis tigrinus 28 26 (92.9) 1,686 2–237 64.8
Elaphe rufodorsata 15 12 (80.0) 396 1–125 33.0
Total 81 61 (75.3) 2,437 1–237 37.7
When we analyzed infection sites of sparganosis cases in the human body (438 cases), subcutaneous tissues were the most commonly affected sites (49.9%; 223 cases), followed by the CNS (36.2%; 162 patients) including the spinal cord. Infection of visceral organs was recognized in 7.6% of patients (34 cases). Ocular cases were observed in 16 patients (3.6%). Muscular sparganosis was recorded in 12 patients (2.7%) (Fig. 3). A total number of affected sites exceeded 438 due to infections at multiple sites in seven patients (four cases of subcutaneous and muscular infections, two each case with subcutaneous and visceral infections, and one case of systemic infection).
Fig. 3

Number and sex distribution of cases according to infection sites.

CNS = central nervous system.
aCNS sparganosis included spinal cord infection; bTotal number of cases exceeded 438 due to infections at multiple sites in 7 cases (4 cases of subcutaneous and muscular infections, 2 cases with subcutaneous and visceral infections, and 1 case of systemic sparganosis).
jkms-33-e273-g003

Subcutaneous sparganosis

Sparganosis of subcutaneous tissues was most commonly described in Korea, similar to that observed in other countries.4192021 Table 3 depicts localities of lesions in the body, number of cases and gender/age distributions among 218 subcutaneous sparganosis reported in Korea (total number was 223 due to multiple infections). We were able to trace medical records of 202 patients, in which men constituted 68.3% (138/202 cases). The most frequently affected site was the lower extremity (35%), followed by trunk (26%). Involvement of the scrotum was observed in 11.7% of men. In women, breast was the most predilection site (34.2%). Clinical and imaging findings of breast sparganosis have previously been summarized.22 Major symptoms of subcutaneous sparganosis included painless mass (91 cases) and painful mass (39 patients). Other symptoms included itching sensation of the infected sites (23 cases) and hemorrhagic mass (5 patients). Some cases with scrotal sparganosis were associated with Fournier's gangrene (19.2%; 5/26 patients). Eleven patients did not complain of any symptom. We could not trace clinical information for 44 patients. Cases with subcutaneous sparganosis were largely detected in the sixth decade (age distribution, 4–85 years). However, a 4-year-old boy and a 6-year-old boy who visited a clinic with chief complaint of a painful neck mass and a painless cystic mass on the scrotum, respectively, were found to be infected with sparganum. The boy who had a neck mass had no history of exposing to any possible infection source while the other boy with scrotal mass had a history of drinking water from mineral springs.2324
Table 3

Number of subcutaneous sparganosis patients in each body compartment along with sex and age distribution

jkms-33-e273-i003
Localities No. of cases (%) Male Female Sex, not-available Age distribution (mean)
Lower extremities 78 (35.0) 55 12 11 27–85 (53.2)
Trunk 58 (26.0) 44 7 7 44–75 (58.8)
Breast 39 (17.5) 0 39 0 29–81 (54.7)
Scrotum 26 (11.7) 26 0 0 32–75 (53.0)
Inguinal area 6 (2.7) 2 2 2 45–63 (53.0)
Upper extremities 5 (2.2) 3 1 1 40–49 (44.5)
Axilla 4 (1.8) 3 1 0 52–61 (56.5)
Penile shaft 2 (0.9) 2 0 0 36–72 (54)
Neck 2 (0.9) 2 0 0 4–80 (42)
Vulva 2 (0.9) 0 2 0 32–52 (42)
Spermatic cord 1 (0.5) 1 0 0 6 (6.0)
Total 223 (100) 138 64 21 4–81 (47.1)
Plain radiographs of subcutaneous sparganosis often show linear or elongated calcifications. Nodular elongated soft tissue mass shadows might also be observed, but not always.25 US findings include poorly-/well-defined, heterogeneous hypoechoic mass in affected sites and multiple elongated, folded, band-like hypoechoic tracts with serpiginous tubular echogenicity.2526 On CT/MRI, multiple serpiginous tubular tracts having peripheral rim enhancement with perilesional soft tissue edema have been recognized.2728

Sparganosis of the CNS and spinal cord

In Korea, at least 162 cases of CNS involvement including the spinal cord were reported. One case was infected at both CNS and the spinal cord29 while 13 cases were spinal cord infections (Table 4). The proportion of CNS cases was remarkably high in Korea compared to that in other countries.4192021 Since the early 1980s', most cerebral cases were diagnosed preoperatively by specific serological tests together with neuroimaging modalities.912303132 CNS involvement was significantly higher in men (75.9%) than that in women (24.1%) among 116 patients whose demographical information was available. Age of these patients ranged from 6 to 72 years. The third (20.7%), fourth (23.2%), fifth (19.8%), and sixth (19.8%) decades constituted major populations (Fig. 4).
Table 4

Number of cerebral sparganosis cases in Korea

jkms-33-e273-i004
Localities No. of cases (mean ages) Sex, not-available Total
Male Female
CNS 100 (35.1) 39 (37.2) 9 148
Spinal cord 9 (49.3) 3 (42.5) 1 13
CNS + spinal cord 0 1 (42.0) 0 1
Total 109 (42.2) 43 (40.6) 10 162
CNS = central nervous system.
Fig. 4

Age and sex distribution of patients with cerebral sparganosis whose demographic information is available (n = 116).

jkms-33-e273-g004
Neuroimaging findings have demonstrated pathognomonic features of cerebral sparganosis, including white matter hypodensity with adjacent ventricular dilatation, irregular or nodular enhancing lesion, and small punctate calcifications. Cortical atrophy has also been recognized in many patients.30 Contrast images of MRI have better resolution than CT in detecting degenerated tissues.31 On neuroimaging scans taken at follow-up monitoring, location or shape of the enhancing lesion is typically altered, suggesting possible wondering of the worm in the hemisphere. This finding is also highly specific for cerebral sparganosis.31
Major symptoms of 148 CNS patients included seizure (20.9%), headache (12.8%), and hemiparesis (6.8%). Altered mental functions such as cognition difficulty, decreased memory and calculation, and intellectual deterioration were observed in 17 cases (11.5%). In addition, some patients manifested with motor weakness (4.7%). These symptoms were shown to be progressed with wax and wane patterns along with the course of the disease. Two patients (1.4%) underwent status epilepticus. Principal symptoms of spinal sparganosis included voiding difficulty (38.5%), back pain (38.5%), and paresis (23.1%). The patient who had concomitant infections in the CNS and spinal cord presented seizure, signs and symptoms of increased intracranial pressure, facial palsy, hearing loss, voiding difficulty, and paresis of the lower extremities. The patient's symptoms were significantly improved after surgical removal of worms in the cerebellar-pontine angle and in the 3rd–5th lumbar spinal cord together with decompression of communicating hydrocephalus by ventriculoperitoneal shunt operation.29

Visceral sparganosis

Sparganosis of visceral organs were relatively infrequent in Korea (7.8%; 34/438 patients). Patients' ages were between 23 and 70 years (mean: 50.6 years). Ratio of man and woman patients was 4.8:1. As shown in Table 5, worms were found in several different organs/tissues, among which the urogenital system (29.4%), the lung (29.4%), and the intestine (23.5%) were mainly affected organs. In the urogenital system, bladder wall, epididymis, and penile shaft infections were described. A ureteral stone associated with sparganum has been reported.32 Pleural sparganosis could provoke chest pain, pleural effusion, dyspnea, and/or empyema.33 Sparganum infected in the intestinal wall caused obstruction, perforation, or abscess formation. An intraperitoneal mass causing abdominal pain has been reported.34 Imaging scans of patients have revealed poorly defined, heterogeneous mass with increased echogenicity, and/or cavitating mass. In addition, double hypoechoic rings surrounding the mass, i.e., “tubule-in-a-tubule” appearance could be observed.35 One case of pericardial mass presenting recurrent pericardiopleural effusion, chest pain, and dyspnea was reported. The patient consumed raw frog flesh more than 30 times for treatment of thyroid disease. She was treated with three consecutive doses of praziquantel (75 mg/kg/day), after which symptoms and pericardial effusion gradually disappeared. However, follow-up surveillance of the patient's anti-sparganum specific antibody level remained to be strongly positive.36 A sparganosis causing retropharyngeal abscess has been recorded in the literature, while detailed history was unavailable.3
Table 5

Number of patients and lesions of visceral sparganosis reported in Korea

jkms-33-e273-i005
Localities No. of cases (%) Male Female Sex, not-available
Urogenital system 10 (29.4) 9 1 0
Lung 10 (29.4) 7 2 1
Intestine 8 (23.5) 5 1 2
Omentum 2 (5.9) 2 0 0
Liver 1 (2.9) 1 0 0
Heart 1 (2.9) 0 1 0
Peritoneal cavity 1 (2.9) 1 0 0
Retropharynx 1 (2.9) 0 0 1
Total 34 (100) 25 5 4

Ocular sparganosis

In Southeast Asian countries including southern China, large numbers of ocular sparganosis have occurred due mainly to application of traditional poultice to subside sores or edema of inflamed eyes and/or skins.420 However, such types of traditional therapy have not been practiced in Korea,3 which might be responsible for the low incidence of ocular sparganosis in this country. A total of 16 ocular cases (3.6%; 16/438 cases) has been reported (Table 6). Patients' age ranged from 11 to 67 years (man:woman = 3:1). Subconjunctival area was the most predilection site (68.8%), followed by eyelid (25%). Their main clinical symptoms were painless mass with/without itching. One case of intraorbital sparganosis was described in an 11-year-old girl who complained of exophthalmos and itching sensation for a year. Other symptoms such as foreign body sensation, decreased visual acuity, or visual field defect were not observed. The patient was initially diagnosed as intraocular malignancy. During operation, a hard mass tightly adhered to the upper posterior intraorbital wall was resected. A live sparganum was extracted from the lesion. Her mother admitted that she had eaten cooked frog for 2–3 times.37 The worm might have directly invaded into the orbit from the periorbital soft tissue. However, how the sparganum penetrated through the orbital wall surrounded by bony structure remains unknown.
Table 6

Number of patients and localities of ocular sparganosis

jkms-33-e273-i006
Locations No. of cases (%) Male Female Sex, not-available
Subconjunctiva 11 (68.8) 7 2 2
Eyelid 4 (25.0) 2 1 1
Intraorbit 1 (6.3) 0 1 0
Total 16 (100) 9 4 3

Muscular sparganosis

Skeletal muscular tissues are relatively reluctant to allow penetration and migration of the sparganum due to their compact architectural structure. Sparganum was often found between muscles and fascial layers surrounded by fibrous capsule. Sparganosis of the muscular system was barely reported in Korea. A total of 12 cases were recorded, including seven men and three women (mean age, 61 years). Personal information for the remaining two patients was unavailable. Four cases had multiple infections in both subcutaneous tissues and muscles. Those muscular sparganosis cases revealed US findings of poorly defined intramuscular mass with heterogeneous echotextures in affected sites,27 resembling those seen in subcutaneous sparganosis.26 Most patients had a painless lump on the affected site (8 cases). The worm was discovered in the chest wall muscles in two cases and in the neck and trunk muscle in one case each.

Systemic sparganosis

An extremely uncommon case of systemic infections with multiple worms was described in Korea. A woman who complained of palpable mass on the breast visited a hospital. During evaluation of the breast mass, subcutaneous masses on the elbow and thigh were also noticed. Whole body MRI revealed multiple nodules on the subcutaneous fat layer of several organs, including the breast, elbow, thighs, calf, chest walls, abdominal wall, inguinal area, and suprapubic area. Masses in the psoas and gluteus muscles were additionally detected. A total of 16 worms were removed from respective tissues and muscles. She had a history of eating snakes to relieve leg pain 40 years ago.38

Sparganosis of immunocompromised patients

Sparganosis or proliferative sparganosis associated with immunocompromised patients, such as those with acquired immune deficiency syndrome (AIDS), cancer, or allograft recipients have been sporadically detected worldwide. Proliferative sparganosis in immunocompromised patients often result in serious outcomes.394041 We found that at least five sparganosis cases in Korea were associated with immunosuppressed conditions. All these cases were reported in recent 10 years.
The first case was identified in a woman patient. The patient who suffered from invasive ductal carcinoma of the right breast suddenly developed a mass on the ipsilateral breast. US findings compatible to sparganosis were observed. A live sparganum was removed via excisional biopsy.42 The next case was noticed in a man who underwent allogeneic hematopoietic stem cell transplantation for treatment of myelodysplastic syndrome. The patient was treated with a nucleic acid synthase inhibitor (decitabine), after which a hard and movable mass was developed on the left scrotum. Multiple enlargements of regional lymph nodes were also observed. Pelvic MRI suggested a myeloid sarcoma in the subcutaneous fat layer. However, histopathological specimen obtained from biopsy revealed a characteristic feature of sparganosis.43 Two patients who received chemotherapy for treatment of metastatic rectal cancer or B cell lymphoma abruptly developed hemorrhagic plaques on abdomen or growing subcutaneous masses of the chest and abdomen. Biopsied specimen exhibited histological features of sparganosis. Both patients agreed that they ingested cooked snakes several times.4445
Two sparganosis cases were misdiagnosed as tumor metastasis. A patient was treated for metastatic gastric cancer. After third rounds of anticancer medication, a painless mass was detected on the left lower extremity which was suspected to be a skin metastasis. Tissue biopsy demonstrated a sparganum.46 Another case was seen in a breast cancer patient. She received neoadjuvant treatment, after which an axillary nodule was additionally recognized. During curative surgery for breast cancer, axillary lesion was also resected and a viable sparganum was recovered.47

DISCUSSION

Sparganosis has been continuously detected in Korea during the past 90 years, although annual incidence seemed to be decreased in the last 20 years. However, whether the prevalence of the sparganosis has actually decreased remains unclear because most clinicians in Korea now regard sparganosis as no longer reportable disease unless unusual complications/sequelae have been combined. In this respect, the authors identified more than 15 sparganosis cases affecting various organs/tissues, including thyroid gland from samples referred from several hospitals during recent 10 years in Korea (Kong Y., unpublished observation). Some minor fractions of the elderly people still believe that snakes/frogs have special benefits for muscular tonicity and treatment of arthralgia, tuberculosis, and other chronic wasting diseases. They continue to consume snakes/frogs, although they are aware that these types of convention are illegal with a risk of parasitic infections including sparganosis. Many people who like hiking, trekking and climbing sometimes drink unfiltered water. Those cultural habits and social behaviors might be the major limiting factors for terminating sparganosis transmission in this country.
In this study, we analyzed sparganosis cases reported in Korea by mining publicly available databases. During the period between 1924 and 2015, at least 438 cases were described in the literature (Fig. 1). We surmise that many more neglected cases are not reported in the literature. Most patients (80.3%) have a history of ingesting frogs/snakes and/or unfiltered water. Patients were largely detected in their middle ages between the fifth and sixth decades. The disease was more common in men than in women (man:woman = 2.5:1). Subcutaneous tissues of the lower extremities were the most frequently affected sites (Fig. 3). These epidemiological situations were similar to those observed in other countries.4192021 However, Korean sparganosis shows some differences in terms of clinical and epidemiological aspects.
Since the 1980s, most patients were preoperatively diagnosed by imaging modalities combined with serological tests. Many cases of cerebral sparganosis have been detected in a relatively young age group (Fig. 4). Detection of a large number of cerebral sparganosis patients in relatively young age groups between third and fourth decades (43.1%) suggested that they might have severe diseases that led to early visit to clinics. Histological characteristics of the brain parenchyma might be related to early and deleterious symptoms/signs of cerebral sparganosis. Sparganum might migrate more vigorously within the brain parenchyma compared to other body compartments because brain parenchyma is mainly composed of soft tissue that is vulnerable to mechanical damage triggered by the invasive wondering worm. Bioactive molecules secreted by the sparganum including tissue hydrolyzing enzymes might also contribute to further damage to friable brain parenchyma.48 A previous study has indicated that the frontoparietal lobes are frequently affected sites.30 Infection of the occipital lobe alone was indeed rarely observed in this retrospective survey. However, involvement of parietal/parietooccipital/parietotemporal lobes was noticed to some extent.123031 The sparganum might randomly invade the whole hemisphere. It might not have a specifically favored site, but it depends on the size of the lobe.
Ocular sparganosis is relatively infrequent in Korea. Large proportions of woman patients are infected with the sparganum on the breast. Interestingly, we recognized one extremely rare case of systemic sparganosis who had index lesion on the breast. Most cases of sparganosis were caused by a single worm. Sometimes two or more worms were found simultaneously in different localities of the body. However, systemic infections with multiple worms are very rare. Whether multiple worms might have infected the patient at once or accumulation of worms by repeated infection with a single worm during long periods could not be properly evaluated in this patient.38
Sparganosis associated with immunocompromised patients has recently been reported in Korea. It is not certain whether immune status of patients truly affects exacerbation of sparganosis lesions and symptoms/signs. However, under immunocompromised conditions, mechanical activity of the sparganum and bioactive molecules secreted by the worm might accelerate and aggravate local damages. Several species of proteolytic enzymes might actively operate in the course of infection. These molecules might additionally contribute to the deterioration of lesions.4849 Although authentic case of fatal sparganosis related to immune suppression has not been reported in this country, those unfavorable conditions should be kept in mind.
We could not identify genuine proliferative sparganosis cases in Korea, although one case of multiple subcutaneous sparganosis was highly suspected to be infected with proliferative sparganum.50 However, proliferative sparganosis has been described in several other countries.51525354 Proliferative sparganum (Sparganum proliferum) is a peculiar type of budding sparganum. It is genetically distinct from Spirometra species.55 The parasite may proliferate asexually, branching, and breaking down into numerous segments, each of which has capacity to further develop. Some cases of proliferative sparganosis are associated with immunosuppressed conditions.394041 Occurrence of proliferative sparganosis should be carefully monitored in Korea.
Recent molecular phylogenetic analysis employing mitochondrial cytochrome c1 (cox1) gene has demonstrated that plerocercoid of S. decipiens can trigger human infections in Korea, in addition to plerocercoid of S. erinaceieuropaei.6 The plerocercoid of S. decipiens has also been recovered from Korean terrestrial snakes. Interestingly, all sparganum (n = 904) recovered from snakes were identified as plerocercoid of S. decipiens, but not that of S. erinaceieuropaei.56 When we consider the fact that S. erinaceieuropaei has not been discovered in naturally infected carnivorous hosts,57 S. decipiens might be the responsible species found in the natural sylvatic cycle. These results suggest strongly that sparganum found in human cases should be carefully revisited for their species identification in the near future.
Currently, drugs effective for treating sparganosis are unavailable.58 In this series, we observed that some patients were treated with praziquantel. A few patients seemed to respond to the drug because their symptoms subsided after medication. However, follow-up monitoring of anti-sparganum specific antibody levels demonstrated strong positive reactions,36 suggesting that the sparganum might become dormant in the body, but not eradicated. This situation should be carefully considered when managing patients. Sparganosis of vital organs and/or related to immune suppressions may result in serious consequences. Public health education with regular interview by local health authorities, periodic check-up of suspected cases, continuous monitoring of the prevalence and medical surveillance system through patient-doctor rapport network might be needed in Korea.

ACKNOWLEDGMENTS

The authors are grateful to Ms. Jung-A Kim (Department of Parasitology and Tropical Medicine, Gyeongsang National University College of Medicine) for her excellent assistance during collection of sparganum from snakes.

Notes

Disclosure: The authors have no potential conflicts of interest to disclose.

Author Contributions: Conceptualization: Nawa Y, Kong Y. Data curation: Kim JG, Sohn WM, Nawa Y, Kong Y. Formal analysis: Kim JG, Ahn CS, Kong Y. Writing - original draft: Kim JG, Kong Y. Writing - review & editing: Ahn CS, Sohn WM, Nawa Y, Kong Y.

References

1. Lee SH, Chai JY, Seo BS, Cho SY. Two cases of human infection by adult of Spirometra erinacei. Korean J Parasitol. 1984; 22(1):66–71.
2. Weinstein PP, Krawczyk HJ, Peers JH. Sparganosis in Korea. Am J Trop Med Hyg. 1954; 3(1):112–129. PMID: 13114596.
crossref
3. Cho SY, Bae JH, Seo BS. Some aspects of human sparganosis in Korea. Korean J Parasitol. 1975; 13(1):60–77.
crossref
4. Liu Q, Li MW, Wang ZD, Zhao GH, Zhu XQ. Human sparganosis, a neglected food borne zoonosis. Lancet Infect Dis. 2015; 15(10):1226–1235. PMID: 26364132.
crossref
5. Bowman DD, Hendrix CM, Lindsay DS, Barr SC. Feline Clinical Parasitology. 1st ed. Ames, IA: Iowa State University Press;2002.
6. Jeon HK, Park H, Lee D, Choe S, Kim KH, Huh S, et al. Human infections with Spirometra decipiens plerocercoids identified by morphologic and genetic analyses in Korea. Korean J Parasitol. 2015; 53(3):299–305. PMID: 26174823.
7. Kong Y, Cho SY, Kang WS. Sparganum infections in normal adult population and epileptic patients in Korea: a seroepidemiologic observation. Korean J Parasitol. 1994; 32(2):85–92. PMID: 8025037.
crossref
8. Lee KJ, Bae YT, Kim DH, Deung YK, Ryang YS. A seroepidemiologic survey for human sparganosis in Gangweon-do. Korean J Parasitol. 2002; 40(4):177–180. PMID: 12509101.
crossref
9. Kim H, Kim SI, Cho SY. Serological diagnosis of human sparganosis by means of micro-ELISA. Korean J Parasitol. 1984; 22(2):222–228.
crossref
10. Doi T, Boku S. The first case of Sparganum mansoni from a Korean and three cases from Japanese. J Chosen Med Ass. 1924; 50:47–51.
11. Min DY. Cestode infections in Korea. Korean J Parasitol. 1990; 28(Suppl):123–144.
crossref
12. Chang KH, Cho SY, Chi JG, Kim WS, Han MC, Kim CW, et al. Cerebral sparganosis: CT characteristics. Radiology. 1987; 165(2):505–510. PMID: 3659374.
crossref
13. Chung SY, Park KS, Lee Y, Park CK. Breast sparganosis: mammographic and ultrasound features. J Clin Ultrasound. 1995; 23(7):447–451. PMID: 7560161.
crossref
14. Cho SY, Kang SY, Kong Y. Purification of antigenic protein of sparganum by immunoaffinity chromatography using a monoclonal antibody. Korean J Parasitol. 1990; 28(3):135–142.
crossref
15. Morakote N, Kong Y. Antigen specificity of 36 and 31 kDa proteins of Spirometra erinacei plerocercoid in tissue invading nematodiasis. Korean J Parasitol. 1993; 31(2):169–171. PMID: 7688246.
16. Kobayashi H. On the animal parasites in Korea. Jpn Med World. 1925; 5(1):9–16.
17. Cho SY, Hwang KI, Seo BS. On the Sparganum mansoni infection in some Korean terrestrial snakes. Korean J Parasitol. 1973; 11(2):87–94.
18. Kim CH. The infection status of sparganum and Gnathostoma in frogs of southern part of Korea. Korean J Parasitol. 1983; 21(1):83–86.
19. Mitchell A, Scheithauer BW, Kelly PJ, Forbes GS, Rosenblatt JE. Cerebral sparganosis. Case report. J Neurosurg. 1990; 73(1):147–150. PMID: 2191089.
20. Anantaphruti MT, Nawa Y, Vanvanitchai Y. Human sparganosis in Thailand: an overview. Acta Trop. 2011; 118(3):171–176. PMID: 21459073.
crossref
21. Lo Presti A, Aguirre DT, De Andrés P, Daoud L, Fortes J, Muñiz J. Cerebral sparganosis: case report and review of the European cases. Acta Neurochir (Wien). 2015; 157(8):1339–1343. PMID: 26085111.
crossref
22. Koo M, Kim JH, Kim JS, Lee JE, Nam SJ, Yang JH. Cases and literature review of breast sparganosis. World J Surg. 2011; 35(3):573–579. PMID: 21203758.
crossref
23. Lee EG, Kim WJ, Lee HJ, Lee SE, Yoon MS. Sparganosis in a child. Korean J Dermatol. 2012; 50(12):1087–1088.
24. Lim D, Kim CS, Kim SI. Sparganosis presenting as spermatic cord hydrocele in six-year-old boy. Urology. 2007; 70(6):1223.e1–1223.e2.
crossref
25. Kim HY, Kang CH, Kim JH, Lee SH, Park SY, Cho SW. Intramuscular and subcutaneous sparganosis: sonographic findings. J Clin Ultrasound. 2008; 36(9):570–572. PMID: 18431747.
crossref
26. Choi SJ, Park SH, Kim MJ, Jung M, Ko BH. Sparganosis of the breast and lower extremities: sonographic appearance. J Clin Ultrasound. 2014; 42(7):436–438. PMID: 24633936.
crossref
27. Cho JH, Lee KB, Yong TS, Kim BS, Park HB, Ryu KN, et al. Subcutaneous and musculoskeletal sparganosis: imaging characteristics and pathologic correlation. Skeletal Radiol. 2000; 29(7):402–408. PMID: 10963426.
crossref
28. Ha S, Oh SW, Kim YK, Yi A, Ahn YJ. Breast sparganosis incidentally detected by FDG PET/CT. Nucl Med Mol Imaging. 2013; 47(2):130–133. PMID: 24900094.
crossref
29. Yoo H, Kim DG. Sparganosis of brain and lumbar spinal canal. J Korean Neurosurg Soc. 1999; 28(7):1027–1031.
30. Chang KH, Chi JG, Cho SY, Han MH, Han DH, Han MC. Cerebral sparganosis: analysis of 34 cases with emphasis on CT features. Neuroradiology. 1992; 34(1):1–8. PMID: 1553030.
crossref
31. Moon WK, Chang KH, Cho SY, Han MH, Cha SH, Chi JG, et al. Cerebral sparganosis: MR imaging versus CT features. Radiology. 1993; 188(3):751–757. PMID: 8351344.
crossref
32. Kim HW, Kim JH. A case of sparganosis infesting with stone in human ureter. Korean J Urol. 1970; 11(1):23–26.
33. Kim DH, Yi IH, Youn HC, Kim SC, Kim BS, Cho KS, et al. Pleural sparganosis: a case report. Korean J Thorac Cardiovasc Surg. 2006; 39(6):502–503.
34. Lee JH, Yu JS, Park MS, Lee SI, Yang SW. Abdominal sparganosis presenting as an abscess with fistulous communication to the bowel. AJR Am J Roentgenol. 2005; 185(4):1084–1085. PMID: 16177444.
crossref
35. Park WH, Shin TY, Yoon SM, Park SH, Kang YJ, Kim DK, et al. A case report of testicular sparganosis misdiagnosed as testicular tumor. J Korean Med Sci. 2014; 29(7):1018–1020. PMID: 25045238.
crossref
36. Lee JH, Kim GH, Kim SM, Lee SY, Lee WY, Bae JW, et al. A case of sparganosis that presented as a recurrent pericardial effusion. Korean Circ J. 2011; 41(1):38–42. PMID: 21359068.
crossref
37. Shin JH, Chung JK, Kim WB, Kim DJ, Ok YC, Lee KW. A case report of sparganosis of the orbit. J Korean Neurosurg Soc. 1975; 4(2):409–412.
38. Song EJ, Sohn YM, Ryu KN, Min SY, Shin SH, Park YK. Breast sparganosis and incidentally detected subcutaneous and intramuscular sparganosis at several sites: case report and literature review. Jpn J Radiol. 2015; 33(4):225–228. PMID: 25725936.
crossref
39. Connor DH, Sparks AK, Strano AJ, Neafie RC, Juvelier B. Disseminated parasitosis in an immunosuppressed patient. Possibly a mutated sparganum. Arch Pathol Lab Med. 1976; 100(2):65–68. PMID: 803199.
40. Olson PD, Yoder K, Fajardo L-G LF, Marty AM, van de Pas S, Olivier C, et al. Lethal invasive cestodiasis in immunosuppressed patients. J Infect Dis. 2003; 187(12):1962–1966. PMID: 12792874.
crossref
41. Meric R, Ilie MI, Hofman V, Rioux-Leclercq N, Michot L, Haffaf Y, et al. Disseminated infection caused by Sparganum proliferum in an AIDS patient. Histopathology. 2010; 56(6):824–828. PMID: 20546351.
42. Lee YJ, Choo KS, Bae YT, Kim JY. A case report of breast sparganosis in a patient with ipsilateral breast cancer: MRI and ultrasonographic findings. J Korean Soc Radiol. 2010; 63(6):569–575.
crossref
43. Yeo JY, Han JY, Lee JH, Park YH, Lim JH, Lee MH, et al. A case of inguinal sparganosis mimicking myeloid sarcoma. Korean J Parasitol. 2012; 50(4):353–355. PMID: 23230335.
crossref
44. Chun SM, Yun SJ, Lee JB, Lee SC, Won YH, Kim SJ. A case of sparganosis in a patient with rectal cancer. Korean J Dermatol. 2012; 50(4):332–336.
45. Roh SY, Lee JY, Park KW, Jung SN. Sparganosis in a patient with diffuse large B cell lymphoma. J Cancer Res Ther. 2013; 9(4):712–714. PMID: 24518723.
crossref
46. Lee JS, Park SJ, Park MI, Kim KJ, Moon W, Shin EK, et al. A case of sparganosis mimicking a skin metastasis in a patient with stomach cancer. Korean J Med. 2009; 77(6):755–758.
47. Lee EK, Yoo YB. Axillary sparganosis which was misunderstood lymph node metastasis during neoadjuvant chemotheraphy in a breast cancer patient. Ann Surg Treat Res. 2014; 87(6):336–339. PMID: 25485243.
crossref
48. Kong Y, Chung YB, Cho SY, Choi SH, Kang SY. Characterization of three neutral proteases of Spirometra mansoni plerocercoid. Parasitology. 1994; 108(Pt 3):359–368. PMID: 8022661.
49. Kong Y, Chung YB, Cho SY, Kang SY. Cleavage of immunoglobulin G by excretory-secretory cathepsin S-like protease of Spirometra mansoni plerocercoid. Parasitology. 1994; 109(Pt 5):611–621. PMID: 7831096.
50. Cho BK, Chun CS, Choi WY, Cho SY. A case of unusual sparganosis. Korean J Dermatol. 1985; 23(5):672–677.
51. Torres JR, Noya OO, Noya BA, Mouliniere R, Martinez E. Treatment of proliferative sparganosis with mebendazole and praziquantel. Trans R Soc Trop Med Hyg. 1981; 75(6):846–847. PMID: 7330947.
crossref
52. Moulinier R, Martinez E, Torres J, Noya O, de NOya BA, Reyes O. Human proliferative sparganosis in Venezuela: report of a case. Am J Trop Med Hyg. 1982; 31(2):358–363. PMID: 7072899.
53. Lo YK, Chao D, Yan SH, Liu HC, Chu FL, Huang CI, et al. Spinal cord proliferative sparganosis in Taiwan: a case report. Neurosurgery. 1987; 21(2):235–238. PMID: 3309711.
crossref
54. Nakamura T, Hara M, Matsuoka M, Kawabata M, Tsuji M. Human proliferative sparganosis. A new Japanese case. Am J Clin Pathol. 1990; 94(2):224–228. PMID: 2196778.
crossref
55. Jeon HK, Park H, Lee D, Choe S, Sohn WM, Eom KS. Molecular detection of Spirometra decipiens in the United States. Korean J Parasitol. 2016; 54(4):503–507. PMID: 27658603.
56. Jeon HK, Park H, Lee D, Choe S, Kim KH, Sohn WM, et al. Genetic identification of Spirometra decipiens plerocercoids in terrestrial snakes from Korea and China. Korean J Parasitol. 2016; 54(2):181–185. PMID: 27180576.
57. Faust EC, Campbell HE, Kellogg CR. Morphological and biological studies on the species of Diphyllobothrium in China. Am J Hyg. 1929; 9(3):560–583.
58. Wittner M, Tanowitz HB. Other cestode infection. In : Guerrant RL, Walker DH, Weller PF, editors. Essentials of Tropical Infectious Disease. New York, NY: Churchill Livingstone;2001. p. 490–491.
TOOLS
ORCID iDs

Jeong-Geun Kim
https://orcid.org/0000-0002-4162-5109

Chun-Seob Ahn
https://orcid.org/0000-0001-7719-4817

Woon-Mok Sohn
https://orcid.org/0000-0002-9795-9386

Yukifumi Nawa
https://orcid.org/0000-0002-0206-5196

Yoon Kong
https://orcid.org/0000-0003-0905-4606

Similar articles