• View in gallery
    Figure 1.

    (A) Incidental liver finding. Computed tomography (CT) scan of a hypodense mass (arrow) in liver segment VII, measuring approximately 2.4 cm in width, and undergoing heterogenous enhancement after intravenous injection of contrast material. (B) A positron emission tomography (PET) revealing mild 18F-fluorodeoxyglucose (FDG) uptake (arrow), measuring a maximal standardized uptake value (SUVmax) of 3.1. ( C) A magnetic resonance imaging (MRI) further detailed the lesion (arrow) as mostly non-enhancing following gadolinium injection, but also not showing cystic or necrotic patterns on T2. Additionally, there was no diffusion restriction in the lesion. This figure appears in color at www.ajtmh.org.

  • View in gallery
    Figure 2.

    (A) Eosinophilic palisaded granuloma in liver. Central necrosis (left) and inflamed liver parenchyma (right), separated by (arrows) a rim of histiocytes, eosinophils, and lymphocytes (H&E, original magnification ×40). (B) Transverse section through a degenerated/necrotic larva (arrows), resembling Capillaria hepatica (H&E, original magnification ×100). This figure appears in color at www.ajtmh.org.

  • 1.

    Fuehrer HP , Igel P , Auer H , 2011. Capillaria hepatica in man—an overview of hepatic capillariosis and spurious infections. Parasitol Res 109: 969979.

    • Search Google Scholar
    • Export Citation
  • 2.

    Borba VH , Machado-Silva JR , Le Bailly M , Iñiguez AM , 2019. Worldwide paleodistribution of capillariid parasites: paleoparasitology, current status of phylogeny and taxonomic perspectives. PLoS One 14: 119.

    • Search Google Scholar
    • Export Citation
  • 3.

    Strand TM , Lundkvist Å , 2019. Rat-borne diseases at the horizon, a systematic review on infectious agents carried by rats in Europe 1995–2016. Infect Ecol Epidemiol 9, doi: 10.1080/20008686.2018.1553461.

    • Search Google Scholar
    • Export Citation
  • 4.

    Da Rocha EJG , De Almeida Basano S , De Souza MM , Honda ER , De Castro MB , Colodel EM , Silva JCDE , Barros LP , Rodrigues ES , Camargo LMA , 2015. Study of the prevalence of Capillaria hepatica in humans and rodents in an urban area of the city of Porto Velho, Rondônia, Brazil. Rev Inst Med Trop São Paulo 57: 3946.

    • Search Google Scholar
    • Export Citation
  • 5.

    Yadav SC , Sathe PA , Ghodke RK , 2016. Hepatic capillariasis: a rare parasitic infection. Indian J Pathol Microbiol 59: 124125.

  • 6.

    Cabada MM , Lopez M , White AC , 2013. Capillaria hepatica pseudoinfection. Am J Trop Med Hyg 89: 609.

  • 7.

    McQuown AL , 1950. Capillaria hepatica; report of genuine and spurious cases. Am J Trop Med Hyg 30: 761767.

  • 8.

    Pereira VG , Mattosinho Franca LC , 1983. Successful treatment of Capillaria hepatica infection in an acutely ill adult. Am J Trop Med Hyg 32: 12721274.

    • Search Google Scholar
    • Export Citation
  • 9.

    Li CD , Yang HL , Wang Y , 2010. Capillaria hepatica in China. World J Gastroenterol 16: 698702.

  • 10.

    Kaplan KJ , Goodman ZD , Ishak KG , 2001. Eosinophilic granuloma of the liver: a characteristic lesion with relationship to visceral larva migrans. Am J Surg Pathol 25: 13161321.

    • Search Google Scholar
    • Export Citation
  • 11.

    Juncker-Voss M , Prosl H , Lussy H , Enzenberg U , Auer H , Nowotny N , 2000. Serological detection of Capillaria hepatica by indirect immunofluorescence assay. J Clin Microbiol 38: 431433.

    • Search Google Scholar
    • Export Citation
  • 12.

    Else KJ , Keiser J , Holland CV , Grencis RK , Sattelle DB , Fujiwara RT , Bueno LL , Asaolu SO , Sowemimo OA , Cooper PJ , 2020. Whipworm and roundworm infections. Nat Rev Dis Primers 6, doi: 10.1038/s41572-020-0171-3.

    • Search Google Scholar
    • Export Citation
  • 13.

    Wong SSY , Poon RWS , To KKW , Chan JFW , Lu G , Xing F , Cheng VCC , Yuen KY , 2019. Improving the specific diagnosis of trematode, cestode and nematode infections by a multiplex single-tube real-time PCR assay. J Clin Pathol 72: 487492.

    • Search Google Scholar
    • Export Citation
  • 14.

    Mattiucci S , Paoletti M , Borrini F , Palumbo M , Palmieri RM , Gomes V , Casati A , Nascetti G , 2011. First molecular identification of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infect Dis 11: 82.

    • Search Google Scholar
    • Export Citation
  • 15.

    Powers TO , Neher DA , Mullin P , Esquivel A , Giblin-Davis RM , Kanzaki N , Stock SP , Mora MM , Uribe-Lorio L , 2009. Tropical nematode diversity: vertical stratification of nematode communities in a Costa Rican humid lowland rainforest. Mol Ecol 18: 985996.

    • Search Google Scholar
    • Export Citation
  • 16.

    Guardone L , Deplazes P , Macchioni F , Magi M , Mathis A , 2013. Ribosomal and mitochondrial DNA analysis of Trichuridae nematodes of carnivores and small mammals. Vet Parasitol 197: 364369.

    • Search Google Scholar
    • Export Citation
  • 17.

    Williams SH et al. 2019. Discovery of two highly divergent negative-sense RNA viruses associated with the parasitic nematode, Capillaria hepatica, in wild Mus musculus from New York City. J Gen Virol 100: 13501362.

    • Search Google Scholar
    • Export Citation
  • 18.

    Wilamowski A , Moran S , Greenburg Z , 2002. Commensal Rodents and Their Parasites in Israel. Proceedings of the 4th International Conference on Urban Pests, 103– 112.

  • 19.

    Fuehrer HP , 2014. An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 1—muroidea. Parasitol Res 113: 619640.

    • Search Google Scholar
    • Export Citation
  • 20.

    Fuehrer HP , 2014. An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 2—mammalia (excluding muroidea). Parasitol Res 113: 641651.

    • Search Google Scholar
    • Export Citation
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Capillaria hepatica (syn. Calodium hepaticum) as a Cause of Asymptomatic Liver Mass

Uri Manor Sheba Medical Center, Ramat Gan, Israel;
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel;

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Victoria Doviner Shaare Zedek Medical Center, Jerusalem, Israel;
The Hebrew University School of Medicine, Jerusalem, Israel;

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Jolanta Kolodziejek University of Veterinary Medicine Vienna, Vienna, Austria;

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Pia Weidinger University of Veterinary Medicine Vienna, Vienna, Austria;

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Amir Dagan Shaare Zedek Medical Center, Jerusalem, Israel;
The Hebrew University School of Medicine, Jerusalem, Israel;

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Menahem Ben-Haim Shaare Zedek Medical Center, Jerusalem, Israel;
The Hebrew University School of Medicine, Jerusalem, Israel;

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Merav Rokah Sheba Medical Center, Ramat Gan, Israel;
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel;

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Norbert Nowotny University of Veterinary Medicine Vienna, Vienna, Austria;
College of Medicine, Mohammed Bin Rashid University of Medicine and Health Sciences, Dubai, United Arab Emirates

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Daniel Boleslavsky Sheba Medical Center, Ramat Gan, Israel;
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel;

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Abstract.

Capillaria hepatica (syn. Calodium hepaticum) is a parasitic nematode of rodents, rarely infecting humans. An asymptomatic Israeli adult male with extensive travel history was diagnosed with a liver mass on routine post-thymectomy follow-up. Imaging and computer tomography (CT) guided biopsy were inconclusive. Surgical excision revealed an eosinophilic granuloma with fragments of a nematode suspected to be C. hepatica. Molecular methods verified the diagnosis, and the patient was treated empirically. This is the first case of hepatic capillariasis described in Israel, and the first to be diagnosed using molecular methods.

Capillaria hepatica is a parasitic nematode whose main host are rodents. It is known to paratenically infect livers of various mammals, including, rarely, humans. It has a remarkable affinity to liver tissue, where it matures, mates, and lays eggs. Eggs are released to the environment only via death of the host. 1 As a ubiquitous parasite of a ubiquitous host, C. hepatica is found worldwide. In a recent systematic review of worldwide paleodistribution of capillariid parasites, C. hepatica ova were the most frequently identified. 2 Furthermore, an extensive systematic review of rat-borne infectious agents in Europe indicated C. hepatica as exceptionally widespread and common alongside more renowned pathogens such as Leptospira spp., Hymenolepsis spp., Toxoplasma gondii, and Escherichia coli. 3 Accordingly, human infection has been described in all six continents except Antarctica.

Capillariasis from C. hepatica is considered a rare, underdiagnosed, and neglected human disease, with approximately 200 cases published to date. 1,4,5 It has a slight preponderance for children, and it is still mainly diagnosed in autopsies or incidentally. Poor hygiene and contact with rodents or other animals are thought to be the main risk factors for human infestation; in children, the major cause of infection is pica (eating sand). Infections can lead to hepatic capillariasis, manifesting with the triad of fever, hepatic masses, and eosinophilic leukocytosis. Alternatively, they can manifest as visceral larva migrans (VLM) or asymptomatically. The disease can be fatal in humans, as transmission of the parasite depends on death of the definite host. 1 Spurious infections (i.e., incidental identification of C. hepatica ova in feces) have also been described. 6,7 The cornerstone of treatment are anti-helminthic drugs, especially benzimidazoles (e.g., albendazole, mebendazole). Adjunctive corticosteroids have also been used. 8

Diagnostic imaging is not specific and usually warrants tissue sampling. 9 To date, definitive diagnosis is based almost solely on histopathological examination of suspicious or incidentally encountered liver masses. Typical findings include multiple eosinophilic granulomas with central necrosis, and results may include fragments of nematodes and/or ova. Adult worms are 2.3–4.3 mm long and have a diameter of ≥ 50 μm. Larva vary in size according to stage. Eggs are 40–67 μm × 27–35 μm in size. 10 Serological identification using indirect immunofluorescence of human serum has been described, but this method has not evolved into common practice, probably owing to the rarity of the disease and low index of suspicion. 11 The histological diagnosis of helminth infection poses a challenge to pathologists, and serology tests have inherent limitations. Thus, molecular methods (which are already standard in bacteriology and protozoology) are urgently needed also in blood and tissue specimens suspicious for parasites. 12 For example, Wong et al. developed a multiplex test for various helminths in several biologic media, and Mattiucci et al. described molecular identification of Anisakis pegreffii in intestinal granulomas. 13,14 We are not aware of published molecular diagnosis tools for capillariasis in humans.

A 59-year-old male underwent yearly computed tomography (CT) scans as follow-up for a thymectomy 4 years prior because of a stage I type AB thymoma. On his most recent CT (Figure 1A), a new hypodense mass was detected in liver segment VII, measuring approximately 2.4 cm in width, and undergoing heterogeneous enhancement after intravenous injection of contrast material. A positron emission tomography (PET) was conducted (Figure 1B), revealing mild 18F-fluorodeoxyglucose (FDG) uptake in the lesion, measuring a maximal standardized uptake value (SUVmax) of 3.1. A magnetic resonance imaging (MRI, Figure 1C) further detailed the lesion as mostly nonenhancing after gadolinium injection, but also not showing cystic or necrotic patterns on T2. Additionally, there was no diffusion restriction in the lesion. No other lesions were found by imaging. Multidisciplinary consultation recommended a biopsy, which was inconclusive, and surgery was scheduled. During surgery, a multilobulated firm 3 cm lesion was found, and a segmental hepatectomy was done.

Figure 1.
Figure 1.

(A) Incidental liver finding. Computed tomography (CT) scan of a hypodense mass (arrow) in liver segment VII, measuring approximately 2.4 cm in width, and undergoing heterogenous enhancement after intravenous injection of contrast material. (B) A positron emission tomography (PET) revealing mild 18F-fluorodeoxyglucose (FDG) uptake (arrow), measuring a maximal standardized uptake value (SUVmax) of 3.1. ( C) A magnetic resonance imaging (MRI) further detailed the lesion (arrow) as mostly non-enhancing following gadolinium injection, but also not showing cystic or necrotic patterns on T2. Additionally, there was no diffusion restriction in the lesion. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene 105, 1; 10.4269/ajtmh.21-0120

Histological examination revealed necrotizing eosinophilic granulomas (Figure 2A), with central necrotic zones showing debris of hepatocytes, mixed inflammatory infiltrates (mainly eosinophils), and multiple Charcot–Leyden crystals. In addition, several sections of whole degenerated/necrotic larva were detected (Figure 2B). The parasite measured up to 53 μm in diameter, and it resembled C. hepatica.

Figure 2.
Figure 2.

(A) Eosinophilic palisaded granuloma in liver. Central necrosis (left) and inflamed liver parenchyma (right), separated by (arrows) a rim of histiocytes, eosinophils, and lymphocytes (H&E, original magnification ×40). (B) Transverse section through a degenerated/necrotic larva (arrows), resembling Capillaria hepatica (H&E, original magnification ×100). This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene 105, 1; 10.4269/ajtmh.21-0120

Subsequently, the patient was sent to a travel medicine clinic. He was completely asymptomatic. He lived in an urban area, worked as a businessman, and his travel history revealed extensive work-related travel during the past years to various European countries, the USA, Maldives, and China. He did not recall any illnesses after his travels, and a review of his past medical records did not reveal any event of eosinophilia or elevated liver enzymes. He had no specific animal contacts. A working diagnosis of VLM on account of C. hepatica or Toxocara spp. was made. He received an empiric course of albendazole (400 mg bid for 14 days), and Toxocara serology (western blot; LDBio Diagnostics, France) was requested and soon returned negative. Formalin-fixed, paraffin-embedded tissue was sent for experimental molecular identification to the University of Veterinary Medicine, Vienna, Austria.

Sample slices were first deparaffinized with xylene and washed twice with absolute ethanol. The air-dried tissue pellet was then incubated with Proteinase K (Qiagen, Hilden, Germany) and ATL tissue lysis buffer (Qiagen) at 55°C until it was completely dissolved. Then 200 µL of the dissolved tissue was processed by an automated nucleic acid (DNA + RNA) extraction system employing QIAamp Viral RNA Mini Kit in a QIAcube device (both Qiagen). For detection of C. hepatica DNA, several PCRs were performed using GoTaq® G2 PCR master mix (Promega, Germany) and four published primer pairs. 13,1517 Potential PCR products were visualized by high-resolution capillary electrophoresis (QIAxcel, Qiagen). However, because none of these PCRs resulted in specific products, three new C. hepatica-specific primer pairs within the highly conserved gene for 18S ribosomal RNA were designed; one of them (233f: 5`-CGGTTCGCTGTTCAGTTGTT-3` / 436r: 5`-TGCTGCCTTCCTTGGATGTA-3`, primer positions according to GenBank acc. no. LC425008) generated reproducible specific amplicons. Subsequent sequencing revealed that the 204 bp long sequence derived from the patient was 100% identical to a C. hepatica sequence (GenBank acc. no. LC425008) that was generated from a liver sample of a common rat (Rattus norvegicus) in Indonesia in 2017.

We describe a rare case of asymptomatic hepatic capillariasis in an adult male, diagnosed histopathologically after a segmental hepatectomy and verified by a novel C. hepatica-specific molecular method. This is the first case of human capillariasis documented in Israel, though its origin (foreign versus local) cannot be defined. C. hepatica has been described both in an Israeli rodent parasite survey, and in several of the patient’s travel destinations. 1820 Helminth infections are still mostly diagnosed by direct observation of parasites and/or ova, probably leading to underdiagnosis or misdiagnosis. Kaplan et al. published a case series of 43 patients with hepatic eosinophilic granulomas, 30% of which were attributed to Toxocara, 5% to C. hepatica, and in 65% of cases, no cause could be identified. 10 Standardized broad-range diagnostic kits could have significant clinical implications, from maximizing identification of helminthic lesions to enabling diagnosis via minimally invasive biopsies, rather than surgical resections, as in the case of our patient. Clinicians should be acquainted with capillariasis as a differential diagnosis of hepatic eosinophilic granulomas, and the evolving option for molecular diagnosis.

REFERENCES

  • 1.

    Fuehrer HP , Igel P , Auer H , 2011. Capillaria hepatica in man—an overview of hepatic capillariosis and spurious infections. Parasitol Res 109: 969979.

    • Search Google Scholar
    • Export Citation
  • 2.

    Borba VH , Machado-Silva JR , Le Bailly M , Iñiguez AM , 2019. Worldwide paleodistribution of capillariid parasites: paleoparasitology, current status of phylogeny and taxonomic perspectives. PLoS One 14: 119.

    • Search Google Scholar
    • Export Citation
  • 3.

    Strand TM , Lundkvist Å , 2019. Rat-borne diseases at the horizon, a systematic review on infectious agents carried by rats in Europe 1995–2016. Infect Ecol Epidemiol 9, doi: 10.1080/20008686.2018.1553461.

    • Search Google Scholar
    • Export Citation
  • 4.

    Da Rocha EJG , De Almeida Basano S , De Souza MM , Honda ER , De Castro MB , Colodel EM , Silva JCDE , Barros LP , Rodrigues ES , Camargo LMA , 2015. Study of the prevalence of Capillaria hepatica in humans and rodents in an urban area of the city of Porto Velho, Rondônia, Brazil. Rev Inst Med Trop São Paulo 57: 3946.

    • Search Google Scholar
    • Export Citation
  • 5.

    Yadav SC , Sathe PA , Ghodke RK , 2016. Hepatic capillariasis: a rare parasitic infection. Indian J Pathol Microbiol 59: 124125.

  • 6.

    Cabada MM , Lopez M , White AC , 2013. Capillaria hepatica pseudoinfection. Am J Trop Med Hyg 89: 609.

  • 7.

    McQuown AL , 1950. Capillaria hepatica; report of genuine and spurious cases. Am J Trop Med Hyg 30: 761767.

  • 8.

    Pereira VG , Mattosinho Franca LC , 1983. Successful treatment of Capillaria hepatica infection in an acutely ill adult. Am J Trop Med Hyg 32: 12721274.

    • Search Google Scholar
    • Export Citation
  • 9.

    Li CD , Yang HL , Wang Y , 2010. Capillaria hepatica in China. World J Gastroenterol 16: 698702.

  • 10.

    Kaplan KJ , Goodman ZD , Ishak KG , 2001. Eosinophilic granuloma of the liver: a characteristic lesion with relationship to visceral larva migrans. Am J Surg Pathol 25: 13161321.

    • Search Google Scholar
    • Export Citation
  • 11.

    Juncker-Voss M , Prosl H , Lussy H , Enzenberg U , Auer H , Nowotny N , 2000. Serological detection of Capillaria hepatica by indirect immunofluorescence assay. J Clin Microbiol 38: 431433.

    • Search Google Scholar
    • Export Citation
  • 12.

    Else KJ , Keiser J , Holland CV , Grencis RK , Sattelle DB , Fujiwara RT , Bueno LL , Asaolu SO , Sowemimo OA , Cooper PJ , 2020. Whipworm and roundworm infections. Nat Rev Dis Primers 6, doi: 10.1038/s41572-020-0171-3.

    • Search Google Scholar
    • Export Citation
  • 13.

    Wong SSY , Poon RWS , To KKW , Chan JFW , Lu G , Xing F , Cheng VCC , Yuen KY , 2019. Improving the specific diagnosis of trematode, cestode and nematode infections by a multiplex single-tube real-time PCR assay. J Clin Pathol 72: 487492.

    • Search Google Scholar
    • Export Citation
  • 14.

    Mattiucci S , Paoletti M , Borrini F , Palumbo M , Palmieri RM , Gomes V , Casati A , Nascetti G , 2011. First molecular identification of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infect Dis 11: 82.

    • Search Google Scholar
    • Export Citation
  • 15.

    Powers TO , Neher DA , Mullin P , Esquivel A , Giblin-Davis RM , Kanzaki N , Stock SP , Mora MM , Uribe-Lorio L , 2009. Tropical nematode diversity: vertical stratification of nematode communities in a Costa Rican humid lowland rainforest. Mol Ecol 18: 985996.

    • Search Google Scholar
    • Export Citation
  • 16.

    Guardone L , Deplazes P , Macchioni F , Magi M , Mathis A , 2013. Ribosomal and mitochondrial DNA analysis of Trichuridae nematodes of carnivores and small mammals. Vet Parasitol 197: 364369.

    • Search Google Scholar
    • Export Citation
  • 17.

    Williams SH et al. 2019. Discovery of two highly divergent negative-sense RNA viruses associated with the parasitic nematode, Capillaria hepatica, in wild Mus musculus from New York City. J Gen Virol 100: 13501362.

    • Search Google Scholar
    • Export Citation
  • 18.

    Wilamowski A , Moran S , Greenburg Z , 2002. Commensal Rodents and Their Parasites in Israel. Proceedings of the 4th International Conference on Urban Pests, 103– 112.

  • 19.

    Fuehrer HP , 2014. An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 1—muroidea. Parasitol Res 113: 619640.

    • Search Google Scholar
    • Export Citation
  • 20.

    Fuehrer HP , 2014. An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 2—mammalia (excluding muroidea). Parasitol Res 113: 641651.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Uri Manor, Sheba Medical Center, Tel HaShomer 5252000, Israel. E-mail: urimanor87@gmail.com

Authors’ addresses: Uri Manor, Merav Rokah, and Daniel Boleslavsky, Sheba Medical Center, Ramat Gan, Israel, and Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel, E-mails: urimanor87@gmail.com, d.daniel.bol@gmail.com, and merv.rok@gmail.com. Victoria Doviner, Amir Dagan, and Menahem Ben-Haim, Shaare Zedek Medical Center, Pathology, Jerusalem, Israel, and The Hebrew University School of Medicine, Jerusalem, Israel, E-mails: victoriad@szmc.org.il, adagan@szmc.org.il, and benhaimm@szmc.org.il. Jolanta Kolodziejek and Pia Weidinger, University of Veterinary Medicine Vienna, Vienna, Austria, E-mails: Jolanta.Kolodziejek@vetmeduni.ac.at and pia.weidinger@vetmeduni.ac.at. Norbert Nowotny, University of Veterinary Medicine Vienna, Vienna, Austria, and College of Medicine, Mohammed Bin Rashid University of Medicine and Health Sciences, Dubai, United Arab Emirates, E-mail: norbert.nowotny@vetmeduni.ac.at.

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