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Lagochilascariasis: case report

Lagoquilascaríase: relato de caso

ABSTRACT

An unusual case of parasitism by Lagochilascaris minor infection is reported in a 38-year-old woman from Paraupebas, Pará, Brazil. The article summarizes the main characteristics of the disease and its etiological agent, including prevalence, life cycle, clinical course and treatment.

Key words:
lagochilascariasis; helminthiasis; parasites; pathology

RESUMO

Relata-se um caso de infecção por Lagochilascaris minor, parasitose incomum, em mulher de 38 anos de idade, procedente de Paraupebas, Pará, Brasil. O artigo resume as principais características da doença e de seu agente etiológico, incluindo prevalência, ciclo de vida, curso clínico e tratamento.

Unitermos:
lagoquilascaríase; helmintíase; parasitos; patologia

INTRODUCTION

Lagochilascariasis is a zoonosis caused by ascaris nematodes of the genus Lagochilascaris. It has five species, including Lagochilascaris minor, which is the only one that causes disease in humans(11 Sprent JFA. Speciation and development in the genus Lagochilascaris. Parasitology. 1971; 62: 71-112., 22 Costa HMA, Silva AVM, Costa PR, Assis SB. Lagochilascaris minor Leiper, 1909 (Nematoda-Ascaridae) de origem humana. Rev Inst Med Trop São Paulo. 1986; 28(2): 126-30.). This worm is exclusively neotropical, and Brazil leads the world's casuistry, with the highest number of cases in the state of Pará(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
).

Leiper reported in 1909 for the first time the nematode L. minor when examining a sample of human origin from Trinidad(44 Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis - a rare helminthic disease. PLoS Negl Trop Dis. 2017; 11(6): e0005510. Available at: https://doi.org/10.1371/journal.pntd.0005510.
https://doi.org/10.1371/journal.pntd.000...
). In his description he calls attention to the cephalic end of helminths, which presents a mouth with three well developed lips, separated by interludes(55 Leiper RT. A new nematode worm from Trinidad: lagochilascaris minor sp. n. Proc Zool Soc (London). 1909; 2: 742-3.). Adult worms measure about 5 to 20 mm and have a white-milky color. Their eggs measure 65 to 85 µm in the largest diameter and have a thick shell, with a coarsely pitted surface containing multiple excavations in "piece meal"(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
).

Artigas et al. described the first case in Brazil in 1968(66 Artigas PT, Araújo P, Romiti N, Ruivo M. Sobre um caso de parasitismo humano por Lagochilascaris minor Leiper, 1909, no Estado de São Paulo, Brasil. Rev Inst Med Trop, São Paulo. 1968; 10: 78-83.) in a 16-year-old female patient from Piracicaba, São Paulo, who had always lived in that state. In 2002, there were 88 cases described in Brazil, 61,3% of them at Para's state(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
).

CASE REPORT

In 2015 a 38-year-old female patient, born in Paraupebas, Pará, Brazil, noticed a painless and slow growing mass of the right cervical region. She presented with fever, phlogistic signs and purulent drainage in the neck, without dysphagia or dyspnea. She sought medical assistance in Belo Horizonte, where she underwent a tonsillectomy and lymphadenectomy.

Anatomopathological examination showed cervical lymph nodes containing cylindrical and white worms measuring on average 1.5 cm in length and 0.1 cm in diameter (Figure 1), which were also present in the tonsil. In histology, there were numerous adult worms with lateral alae and oval-shaped eggs with irregular membrane with a "soda cap" appearance. There were also larvae at various stages of development that were associated with the granulomatous reaction and microabscesses (Figure 2). The morphology of adult worms and eggs led to the diagnosis of lymph node and tonsil lagochilascariasis, a rare parasitism that can be life threatening.

Figure 1
Cervical lymph nodes and adult worms

A) cervical lymph node containing cylindrical worms measuring on average 1.5 cm in length each; B) detail of the lymph node containing the worms.


Figure 2
Histological sections of the lymph node and the tonsil

A) adult worm inside the lymph node (HE, 40×); B) detail of adult worm inside the lymph node, showing the lateral alae (arrow) (HE, 100×); C) note a detail of the Lagochilascaris eggs with "soda cap" appearance (HE, 400×); D) adult worms in the tonsil (HE, 40×).

HE: hematoxylin and eosin.


DISCUSSION

Lagochilascariasis is a parasitosis that is not well known in our country, and the majority of cases are described in the state of Pará, an endemic region of the disease.

According to the existing literature and with experimental cycles, the definitive hosts of this worm would be the felids. They would harbor the adult phase of the parasite in their digestive or respiratory system, where oviposition would occur. The eggs would be eliminated by the feces of these natural hosts, contaminating the soil. Rodents, intermediate hosts, become infected by the ingestion of the embryonated form of these eggs, which become larval form, forming cysts in the muscles of these animals. The cycle closes as the definitive hosts feed on contaminated rodents(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
, 66 Artigas PT, Araújo P, Romiti N, Ruivo M. Sobre um caso de parasitismo humano por Lagochilascaris minor Leiper, 1909, no Estado de São Paulo, Brasil. Rev Inst Med Trop, São Paulo. 1968; 10: 78-83.,77 Moraes MAP, Arnaud MVC, Macedo RC, Anglada AE. Infecção pulmonar fatal por Lagochilascaris sp., provavelmente Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop, São Paulo. 1985; 27(1): 46-52. Available at: http://www.scielo.br/pdf/rimtsp/v27n1/09.pdf.
http://www.scielo.br/pdf/rimtsp/v27n1/09...
) (Figure 3). Human appears to be an accidental host, consuming raw or unhealthy meat from infected wild animals (agouti, tapir, capybara etc.)(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
). The patient, who lived in the area where most cases are recorded in the world, confirmed the ingestion of this type of meat.

Figure 3
Possible biological cycle of Lagochilascaris minor

(A) the infected definitive host (feline) releases worm's eggs (B) which contaminate the soil (C). The intermediate host (D) feeds on contaminated plants and becomes infected. The human enters as an accidental host by ingesting bush meat contaminated with the embryonated eggs of the parasite (E). The passage of the worm through the digestive tract (F) leads to its evolution, followed by a possible pulmonary cycle (G), in which Lagochilascaris ascends through the respiratory tract, migrating toward neighboring regions (H), such as lymph nodes (I) and the central nervous system (J).


There are still doubts about how to explain the preferential location of lesions in humans. The most accepted theory is that the encysted larvae ingested in the raw meat would leave the cysts in the stomach lumen and migrate later through the esophagus to the structures of the neck by a mechanism not clarified yet(88 Campos DM, Freire Filha LG, Vieira MA, Paçô JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper. Rev Inst Med Trop, São Paulo. 2002; 34(4): 277-87.).

Infection in humans causes suppurative tumor lesions in the neck, the mastoid region and the middle ear, and may also affect the lungs and the central nervous system. In these last two places, the disease is serious and potentially life threatening. Cases have also been reported in the paranasal sinuses, dental alveolus, eyeball, temporoparietal-occipital, and sacral region(99 Vieira MA, Oliveira JA, Ferreira LS, Oliveira V, Barbosa CAL. Relato de caso de Lagochilascariase humana procedente do estado do Pará, Brasil. Rev Soc Bras Med Trop, São Paulo. 2000; 33(1): 87-90.). Finding worms in the suppurative lesions is common, a fact not observed in this patient, which made diagnosis difficult.

The pathological process is characterized by a foreign body type granulomatous reaction (Figure 4). There are also abscesses interconnected by fistulous routes with granulation tissue. Multinucleated giant cells and fibrosis are associated(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
,88 Campos DM, Freire Filha LG, Vieira MA, Paçô JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper. Rev Inst Med Trop, São Paulo. 2002; 34(4): 277-87.). During this inflammatory process, adult worms with lateral alae and oval-shaped eggs with irregular membrane with a "soda cap" appearance and larvae in several stages are observed.

Figure 4
Granulomatous reaction around adult worms (HE, 100×)

HE: hematoxylin and eosin.


Clinical diagnosis is rarely performed in the early stages of the disease, as infected individuals seek medical assistance only in the advanced stages. The parasitological diagnosis is based on the discovery of the parasite, obtained from the lesion. There is a similarity between the eggs of L. minor and Ascaris lumbricoides, a fact that requires attention to differentiate them (Figure 5). The Complete Blood Count (CBC) is of small value and may show leukocytosis or leukopenia, presence or absence of eosinophilia(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
, 88 Campos DM, Freire Filha LG, Vieira MA, Paçô JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper. Rev Inst Med Trop, São Paulo. 2002; 34(4): 277-87.).

Figure 5
Comparison between eggs of Ascaris lumbricoides and Lagochilascaris minor

A) the A. lumbricoides egg membrane is regular; B) the L. minor egg membrane is dentate, with "soda cap" appearance.


The disease has a chronic evolution, with phases of recovery and relapses. There are evidence of autoinfection in humans, since all the evolutionary phases of the worm can be found inside the lesions simultaneously(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
).

The severity of the infection depends on the location of the lesion, the ability to reproduce and the incursion of the parasite into the tissues and the immune response of the host(1010 Guimarães VC, Barbosa AP, Camargo LA. Otomastoidite por Lagochilascaris minor em criança: relato de caso. Available at: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1809-48722010000300017#end.
http://www.scielo.br/scielo.php?script=s...
).

The ideal treatment would be an effective drug against eggs, larvae and adult worms and that could also prevent the embryogenesis of the egg. Thiabendazole and levamisole are potent drugs against adult worms and probably effective against larvae as well, however, both drugs are ineffective against eggs. Consequently, eggs may continue to develop and ultimately lead to larval incubation, giving rise to new adult worms and causing new lesions. Prolonged use of anthelmintics associated with surgical management is then advocated. It can be started with thiabendazole, followed by diethylcarbamazine or mebendazole, and finally levamisole. The surgical removal combined with drug usage presents better results(33 Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf.
http://www.scielo.br/pdf/rboto/v68n1/878...
,44 Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis - a rare helminthic disease. PLoS Negl Trop Dis. 2017; 11(6): e0005510. Available at: https://doi.org/10.1371/journal.pntd.0005510.
https://doi.org/10.1371/journal.pntd.000...
,88 Campos DM, Freire Filha LG, Vieira MA, Paçô JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper. Rev Inst Med Trop, São Paulo. 2002; 34(4): 277-87.,1111 Paço JM, Campos DMB. Lagochilascaris minor Leiper, 1909: nove décadas de revisão bibliográfica. Rev Pat Trop. 1998; 27(1): 11-34.).

Relapses are frequent, since the medication can not eliminate all the evolutionary phases present in the lesions, so that autoinfection occurs(44 Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis - a rare helminthic disease. PLoS Negl Trop Dis. 2017; 11(6): e0005510. Available at: https://doi.org/10.1371/journal.pntd.0005510.
https://doi.org/10.1371/journal.pntd.000...
). The patient was treated with anthelmintics, but she was not able to tell which drug and, until now, she is well with no relapses. No other family members presented similar symptoms.

The best way of combating disease is prevention. Therefore, meat from wild animals, especially rodents, should be cooked at 100°C for 10 minutes or frozen at -20°C for 15 days before being prepared for human consumption(44 Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis - a rare helminthic disease. PLoS Negl Trop Dis. 2017; 11(6): e0005510. Available at: https://doi.org/10.1371/journal.pntd.0005510.
https://doi.org/10.1371/journal.pntd.000...
).

CONCLUSION

The correct diagnosis of lagochilascariasis is essential to differentiate it from other diseases, leading to the appropriate and early treatment, avoiding the appearance of the severe forms that affect lungs and the central nervous system.

REFERENCES

  • 1
    Sprent JFA. Speciation and development in the genus Lagochilascaris. Parasitology. 1971; 62: 71-112.
  • 2
    Costa HMA, Silva AVM, Costa PR, Assis SB. Lagochilascaris minor Leiper, 1909 (Nematoda-Ascaridae) de origem humana. Rev Inst Med Trop São Paulo. 1986; 28(2): 126-30.
  • 3
    Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol, São Paulo. 2002; 68(1): 101-5. Available at: http://www.scielo.br/pdf/rboto/v68n1/8780.pdf
    » http://www.scielo.br/pdf/rboto/v68n1/8780.pdf
  • 4
    Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis - a rare helminthic disease. PLoS Negl Trop Dis. 2017; 11(6): e0005510. Available at: https://doi.org/10.1371/journal.pntd.0005510
    » https://doi.org/10.1371/journal.pntd.0005510
  • 5
    Leiper RT. A new nematode worm from Trinidad: lagochilascaris minor sp. n. Proc Zool Soc (London). 1909; 2: 742-3.
  • 6
    Artigas PT, Araújo P, Romiti N, Ruivo M. Sobre um caso de parasitismo humano por Lagochilascaris minor Leiper, 1909, no Estado de São Paulo, Brasil. Rev Inst Med Trop, São Paulo. 1968; 10: 78-83.
  • 7
    Moraes MAP, Arnaud MVC, Macedo RC, Anglada AE. Infecção pulmonar fatal por Lagochilascaris sp., provavelmente Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop, São Paulo. 1985; 27(1): 46-52. Available at: http://www.scielo.br/pdf/rimtsp/v27n1/09.pdf
    » http://www.scielo.br/pdf/rimtsp/v27n1/09.pdf
  • 8
    Campos DM, Freire Filha LG, Vieira MA, Paçô JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper. Rev Inst Med Trop, São Paulo. 2002; 34(4): 277-87.
  • 9
    Vieira MA, Oliveira JA, Ferreira LS, Oliveira V, Barbosa CAL. Relato de caso de Lagochilascariase humana procedente do estado do Pará, Brasil. Rev Soc Bras Med Trop, São Paulo. 2000; 33(1): 87-90.
  • 10
    Guimarães VC, Barbosa AP, Camargo LA. Otomastoidite por Lagochilascaris minor em criança: relato de caso. Available at: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1809-48722010000300017#end
    » http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1809-48722010000300017#end
  • 11
    Paço JM, Campos DMB. Lagochilascaris minor Leiper, 1909: nove décadas de revisão bibliográfica. Rev Pat Trop. 1998; 27(1): 11-34.

Publication Dates

  • Publication in this collection
    Jul-Aug 2018

History

  • Received
    30 May 2018
  • Reviewed
    30 May 2018
  • Accepted
    06 June 2018
  • Published
    20 Aug 2018
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