A co-infection case report of Taenia saginata in a patient with subclinical clonorchiasis confirmed by the combination of diagnostic tools
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Clonorchiasis is the common parasitic infection in the general population of the Republic of Korea, however, taeniasis is scarcely reported recently. Here, we describe a case of co-infection with the cestode T. saginata in a patient with subclinical clonorchiasis diagnosed by a combination of diagnostic tools in Korea.
A 56-year-old man visited the hospital having passed proglottids in his stool for the past two months and brought a stool sample with segments to our hospital. He had no abdominal symptoms, such as nausea, vomiting, abdominal pain, diarrhea, or constipation. He used to consume raw beef and fish frequently. We could not find evidence of gravid proglottids which contain fully developed uteri filled with ova or branched uterine structures, within the submitted sample. To identify the tapeworm species, we carried out molecular analyses on the proglottids. The cox1 and ef1a sequences had a 100% match with those of T. saginata and differed from the sequences of the other Taenia species. Upon examination of stool samples fixed by formalin-ether concentration method, no Taenia species ova were observed in 10 slides. Instead, C. sinensis ova were observed, despite the level of IgG specific to C. sinensis being within the normal range. The patient was treated with praziquantel (25 mg/kg, three times a day) for 3 days, and subsequently C. sinensis ova were not found in his stool.
Our case indicates that a combination of morphological, serological, and molecular diagnostic tools should be used for the accurate diagnosis of subclinical parasitic infections.
KeywordsTaenia saginata Clonorchis sinensis Molecular diagnosis Ova ELISA
Cytochrome c oxidase subunit I
Elongation factor-1 alpha
Enzyme-linked immunosorbent assay
Polymerase chain reaction
Intestinal parasitic infections are still a major public health issue in worldwide . Until the 1970s, many Koreans had intestinal parasitic infections, mostly from soil-transmitted helminthes . Although overall helminth egg-positive rate was 84.3% in the 1st Nationwide Survey , a dramatic decline of the egg-positive rate has been shown to 2.6% in the 8th Nationwide Survey, 2013 . Thus, at present, intestinal parasitic infections are not recognized as a critical problem in Korea. The public health focus has also shifted from soil-transmitted helminthiases to food-borne parasitic infections. Of food-borne parasites, Clonorchis sinensis showed the highest prevalence in Korea showing 2.4% of egg-positive rate in general population . The parasite is more prevalent in populations living by rivers, with an egg-positive rate of 11.4% , as humans usually become infected after ingesting raw or undercooked freshwater fish harboring C. sinensis metacercariae . Human taeniasis, another food-borne parasitic infection, is a zoonotic disease, because it involves pigs (Taenia solium and Taenia asiatica) or cattle (Taenia saginata) as an intermediate host and humans as the definitive host [6, 7]. Studies dating back to 1924 reported Taenia prevalence in Korea at 7.2% or higher [8, 9, 10], but the national prevalence was 1.98% in 1971 . The national prevalence continued to decline, and was reported as 0.004% in 2013 . Here, we describe a case of co-infection case with the cestode T. saginata and the trematode C. sinensis by using a combination of diagnostic tools in a patient with subclinical parasitic infection.
Discussion and conclusions
Human taeniasis is usually diagnosed by observing ova or gravid proglottids in the patient’s stool. From diagnoses conducted after 1993, the Taenia tapeworms infecting humans in Korea were identified as T. solium, T. saginata, and T. asiatica [5, 17, 18]. However, additional differential modalities may be required to clearly distinguish among these species, as morphological characteristics, such as the presence of an unarmed rostellum on the scolex of adult, the large number of uterine twigs, and the presence of a posterior protuberance, can be difficult to observe in individual strobili [17, 18]. Directe sequencing of cox1 sequences have been used to identify the species causing human taeniasis. Cho et al. successfully used cox1 to distinguish between T. saginata and T. asiatica . Recently, studies conducted in China and Lao People’s Democratic Republic reported that hybridization between the three Taenia species cab iccyr, based on sequencing nuclear and mitochondrial genes [19, 20]. In our case, as we did not observe uterine structures or ova in the proglottids in our patient’s stool sample, these proglottids were likely immature. As such, we were unable to identify the tapeworm to the species-level using morphological characters, and thus sequenced both the nuclear gene, ef1a, and the mitochondrial gene, cox1, from the proglottid sample as well. Matches at several polymorphic sites confirmed that the Taenia specimen in this case is most likely T. saginata, and closely related to T. saginata, specimens sampled previously in Korea, China, Indonesia, Thailand and other countries (Fig. 1b and c). Here, we diagnosed that this case of human taeniasis was caused by T. saginata. We confirmed that tapeworm species by sequencing nuclear and mitochondrial gens, which successfully differentiated T. saginata from other Taenia species. Notably, we discovered that co-existence of taeniasis in a patient with subclinical clonorchiasis using a combination of diagnostic tools. Even in the era of molecular tools, the expertise in microscopy is still essential to achieve a correct diagnosis. Further, subclinical clonorchiasis in this case was confirmed only by examining the stool sample using microscopy. Regarding the use of ELISA to diagnose the presence of C. sinensis, ELISA results should be interpreated with caution, as the result can be negative even with an egg-positive [21, 22].
Early documentation of human taeniasis in Korea reported that the prevalence of Taenia was ranging from 7.2 to 12.0% [8, 9, 10]. More recently (2004–2008), the prevalence had declined to low levels of 0–0.01% [3, 23]. Since 2008, there has only been one study that documented four cases of T. saginata, which were diagnosed by sequencing of cox1 . Some researchers have suggested that human taeniasis is now close to absent in Korea, but cases of infection may be hidden, especially in areas where taeniasis was previously ubiguitous. In our case, the patient was from Jeollanam-do, the province with the second highest prevalence of taeniasis after Jeju-do (Island) according to the 1st Nationwide Survey . Co-infection with other parasites can frequently occur in areas with high parasite prevalence, even though the helminthes do not share the same intermediate host . Moreover, people who enjoy eating both raw beef and freshwater fish, as with our patient, have a higher chance of co-infection. The habit of eating raw fish or beef is deeply rooted in traditional customs among residents of rural areas of Korea . In general, educating the public about not eating raw beef and freshwater fish is important for reducing the incidence of food-borne parasitic infections in Korea.
Initially, the patient took albendazole obtained from a pharmacy instead of visiting a hospital, although the medication was not effective. This may be due in part to the National Deworming Campaign in Korea over the past years that focused on soil-transmitted helminthiases and highlighted repeated administration of albendazole to control parasitic infections. An initial 600-mg tablet of praziquantel (10 mg/kg) may be sufficient for treating taeniasis in this case. The patient also received additional praziquantel at a dosage of 75 mg/kg/day for 3 days to treat clonorchiasis. Although we could not find scolex of Taenia species in the submitted specimens, the treatment may have been effective in controlling both taeniasis and clonorchiasis.
In this study, we described an unusual case of co-infection of T. saginata in a patient with subclinical clonorchiasis in Korea. Our results indicate that diagnosis through molecular methods may be helpful in cases with ambiguous morphological characters such as immature proglottids. Overall, a combination of diagnostic tools should be used for the accurate diagnosis of subclinical parasitic infections.
No funding was required for the writing of this case report.
Availability of data and materials
Not applicable (no datasets were analyzed or generated during this study).
KHP participated in the clinical care of the patient. JSJ performed experiments. KIN, SHK and JHS1 advised about and supervised the experiments and interpretations. JHS2 and EJW wrote the manuscript.EJW was responsible for the concept of and critical contribution and revision to this manuscript. JHS1 corresponding to JHS and JHS2 corresponding to JHS. All authors critically reviewed the manuscript for publication. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The collection of fecal samples including tapeworm conducted in accordance with the guidelines and approval of the Institutional Review Board of Chonnam National University Hospital (IRB CNUH-2015-052) and all data analyzed were anonymized. No information was used that could lead to patient identification.
Consent for publication
Written consent to publish this case report was obtained from the patient (Consent No. 2018-P02).
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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