• 1

    Newton RC, Limpuangthip P, Greenberg S, 1992. Strongyloides stercoralis hyperinfection in a carrier of HTLV-I virus with evidence of selective immunosuppression. Am J Med 92 :202–207.

    • Search Google Scholar
    • Export Citation
  • 2

    Gotuzzo E, Terashima A, Alvarez H, 1999. Strongyloides stercoralis hyperinfection associated with human T cell lymphotropic virus type-1 infection in Peru. Am J Trop Med Hyg 60 :146–149.

    • Search Google Scholar
    • Export Citation
  • 3

    Adedayo AO, Grell GA, Bellot P, 2001. Case study: fatal strongyloidiasis associated with human T-cell lymphotropic virus type 1 infection. Am J Trop Med Hyg 65 :650–651.

    • Search Google Scholar
    • Export Citation
  • 4

    Satoh M, Futami A, Takahira K, Kodaira M, Tanaka T, Kuriki K, Hori E, 2003. Severe strongyloidiasis complicated by meningitis and hydrocephalus in an HTLV-1 carrier with increased proviral load. J Infect Chemother 9 :355–357.

    • Search Google Scholar
    • Export Citation
  • 5

    Neva FA, Oliveira J, Gam AA, 1998. Interferon-γ and interleukin-4 responses in relation to serum IgE levels in persons infected with human T lymphotropic virus type I and Strongyloides stercoralis. J Infect Dis 178 :1856–1859.

    • Search Google Scholar
    • Export Citation
  • 6

    Porto MAF, Neva FA, Lisboa W, Thompson R, Alcântara L, Carvalho EM, 2001. HTLV-1 decreases Th2 type of immune response in patients with strongyloidiasis. Parasite Immunol 23 :503–507.

    • Search Google Scholar
    • Export Citation
  • 7

    Porto MAF, Oliveira Filho J, Neva FA, Orge G, Alcântara L, Gam A, Carvalho EM, 2001. Influence of HTLV-1 infection on serologic and skin tests for strongyloidiasis. Am J Trop Med Hyg 65 :610–613.

    • Search Google Scholar
    • Export Citation
  • 8

    Morimoto J, Kaneoka H, Sasatomi Y, Sato YN, Murata T, Ogahara S, Sakata N, 2002. Disseminated strongyloidiasis in nephrotic syndrome. Clin Nephrol 57 :398–401.

    • Search Google Scholar
    • Export Citation
  • 9

    Lemos LB, Qu Z, Laucirica R, Fred HL, 2003. Hyperinfection syndrome in strongyloidiasis: report of two cases. Ann Diagn Pathol 7 :87–94.

    • Search Google Scholar
    • Export Citation
  • 10

    O’Doherty MJ, van de Pette JE, Nunan TO, Croft DN, 1984. Recurrent Strongyloides stercoralis infection in a patient with T-cell lymphoma-leukaemia. Lancet 1 :858.

    • Search Google Scholar
    • Export Citation
  • 11

    Phelps KR, Ginsberg SS, Cinningham AW, Tschachler E, Dosik H, 1991. Case report: adult T-cell leukemia/lymphoma associated with recurrent Strongyloides hyperinfection. Am J Med Sci 302 :224–228.

    • Search Google Scholar
    • Export Citation
  • 12

    Patey O, Gessain A, Breuil J, Courillon-Mallet A, Daniel MT, Miclea JM, Roucayrol AM, Sigaux F, Lafaix C, 1992. Seven years of recurrent severe strongyloidiasis in an HTLV-I-infected man who developed adult T-cell leukaemia. AIDS 6 :575–579.

    • Search Google Scholar
    • Export Citation
  • 13

    Satoh M, Toma H, Sato Y, Takara M, Shiroma Y, Kiyuna S, Hirayama K, 2002. Reduced efficacy of treatment of strongyloidiasis in HTLV-1 carriers related to enhanced expression of IFN-γ and TGF-β1. Clin Exp Immunol 127 :354–359.

    • Search Google Scholar
    • Export Citation

 

 

 

 

ATYPICAL CLINICAL PRESENTATION OF STRONGYLOIDIASIS IN A PATIENT CO-INFECTED WITH HUMAN T CELL LYMPHOTROPHIC VIRUS TYPE I

View More View Less
  • 1 Serviço de Imunologia, Hospital Universitario Professor Edgard Santos, e Faculdade de Farmácia, Universidade Federal da Bahia, Salvador, Bahia, Brazil

Alterations in the immunologic response induced by human T cell lymphotrophic virus type I (HTLV-I) predispose the development of disseminated strongyloidiasis. We report a case of an atypical clinical presentation of strongyloidiasis in a patient co-infected with HTLV-I causing scrotal and perineal pain and infertility. Strongyloides stercoralis was found in the analysis of the sperm and specific therapy for strongyloidiasis was associated with disappearance of the symptoms.

INTRODUCTION

Strongyloidiasis has a worldwide distribution and is one of the most important enteric helminthic infections. Diarrhea, abdominal pain, and less frequently vomiting are the main clinical features of the disease. More recently, an association between human T cell lymphotrophic virus type I (HTLV-I) and disseminated strongyloidiasis has been reported.1–4 This association is due to decreased immunity against Strongyloides stercoralis in patients co-infected with HTLV-I. The high production of interferon-γ (IFN-γ) resulting from HTLV-I infection leads to a decreased synthesis of interleukin-4 (IL-4), IL-5, parasite-specific IgE, and eosinophils, cytokines and cells that are involved in the expulsion and killing of S. stercoralis, respectively.5–7 Herein, we report a patient co-infected with HTLV-I and S. stercoralis who sought medical evaluation for infertility. Upon evaluation, S. stercoralis was detected in the ejaculate mixed with spermatozoa and in the urine.

CASE HISTORY

A 27-year-old man born in Salvador, Bahia, Brazil had sperm and urine analyses performed to evaluate infertility. On clinical evaluation, the patient complained of mild pain in the scrotum and perineal region. He denied having diarrhea, abdominal pain, or vomiting. There was mild edema in the scrotum and a urologic examination found small varicoceles. An ultrasound examination showed no abnormalities in the abdomen, but a scrotal examination confirmed the clinical finding of varicoceles. A spermatogram showed a normal number of spermatozoae with normal motility and a large number of rhabditiform and filariform larvae and young adult female S. stercoralis. Contamination of the sperm by urine was ruled out by the aspect of the material and by the forms of parasite found. While rhabditiform larvae were detected only in the urine, all parasite stages were observed in the sperm. The total peripheral white blood cell count and number of eosinophils were normal. Rhabditiform larvae of S. stercoralis were also observed by urine analysis and in the stool. Because of the atypical presentation of S. stercoralis infection, HTLV-I serology was performed. A diagnosis of HTLV-I infection was made and confirmed by Western blot.7 Cytokines were measured in supernatants of mononuclear cells stimulated and not stimulated with S. stercoralis antigen. The levels of IFN-γ, tumor necrosis factor-α, IL-5, and IL-13 (Table 1) were measured by an enzyme-linked immunosorbent assay sandwich technique (Genzyme Corp., Cambridge, MA) and the results were expressed in picograms per milliliter based on a standard curve generated using recombinant cytokines.

The patient was treated with a single dose of cambendazole (5 mg/kg of body weight). The pain in the scrotum and perineal region and edema resolved and the varicoceles were reduced in size. Strongyloides stercoralis was no longer seen on a spermatogram, but rhabditiform larvae were present in the stool examined two months after therapy. The patient was re-treated with a single dose of ivermectin (200 μg/kg of body weight) and the results of a repeated spermatogram and stool examinations every 2–3 months remained negative for S. stercoralis at one year of follow-up. After therapy, his wife became pregnant, indicating that the infertility had improved.

DISCUSSION

Disseminated S. stercoralis infection is a recognized consequence of immune suppression caused by corticosteroids or cytotoxic drugs.8,9 More recently, severe and recurrent strongyloidiasis has been reported in association with HTLV-I co-infection.1–4,10–12 In disseminated strongyloidiasis, increases in parasite load from autoinfection leads to systemic migration of S. stercoralis to other organs. The lungs, liver, and brain are the most common organs invaded by S. stercoralis, leading to severe clinical disease. Herein, we described a patient who complained of scrotal and perineal pain in whom S. stercoralis was found in a spermogram. The documentation of S. stercoralis larvae and adult worm in the sperm and the improvement of perineal symptoms and signs after specific anti-strongyloides treatment indicated not only the ability of this parasite to infect the genitourinary tract, but also to cause symptoms. Patients co-infected with HTLV-I and S. stercoralis, as observed in this case, have higher levels of IFN-γ and lower levels of IL-5 and IL-13 than patients who are infected with S. stercoralis alone.6 The higher IFN-γ production by lymphocytes in patients infected with HTVL-I and S. stercoralis leads to a decreased S. stercoralis-specific type 2 immune response characterized by low levels of IL-4, IL-5, and IL-13,5,6 cytokines that are critical for the control of S. stercoralis infection. Clinically, patients co-infected with HTLV-I and S. stercoralis may develop severe strongyloidiasis, as well as a low cure rate in response to anti-S. stercoralis drugs.13 This report calls attention to an atypical clinical presentation of S. stercoralis in a patient co-infected with HTLV-I in whom the clinical manifestation was related to the dissemination of S. stercoralis into the genitourinary tract, resulting in infertility and scrotal and perineal pain.

Table 1

Levels of IFN-γ, TNF-α, IL-5, and IL-13 in supernatants of lymphocyte cultures stimulated with Strongyloides stercoralis antigen*

Levels (pg/ml)
CytokinesMediumS. stercoralis antigen
* Peripheral blood mononuclear cells were stimulated with 5 μg/mL of S. stercoralis antigen as previously described.5 IFN-γ = interferon-γ; TNF-α = tumor necrosis factor-α; IL-5 = interleukin-5.
IFN-γ70246
TNF-α00
IL-5185184
IL-13207191

Authors’ addresses: Maria Aurélia F. Porto, Néviton Castro, and Edgar M. Carvalho, Serviço de Imunologia, Hospital Universitario Professor Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil. Lêda M. Alcântara and Marcelo Leal, Faculdade de Farmácia, Universidade Federal da Bahia, Salvador, Bahia, Brazil.

Financial support: This work was supported by the Brazilian National Research Council (CNPq) and Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB). Edgar M. Carvalho is a senior investigator of CNPq.

REFERENCES

  • 1

    Newton RC, Limpuangthip P, Greenberg S, 1992. Strongyloides stercoralis hyperinfection in a carrier of HTLV-I virus with evidence of selective immunosuppression. Am J Med 92 :202–207.

    • Search Google Scholar
    • Export Citation
  • 2

    Gotuzzo E, Terashima A, Alvarez H, 1999. Strongyloides stercoralis hyperinfection associated with human T cell lymphotropic virus type-1 infection in Peru. Am J Trop Med Hyg 60 :146–149.

    • Search Google Scholar
    • Export Citation
  • 3

    Adedayo AO, Grell GA, Bellot P, 2001. Case study: fatal strongyloidiasis associated with human T-cell lymphotropic virus type 1 infection. Am J Trop Med Hyg 65 :650–651.

    • Search Google Scholar
    • Export Citation
  • 4

    Satoh M, Futami A, Takahira K, Kodaira M, Tanaka T, Kuriki K, Hori E, 2003. Severe strongyloidiasis complicated by meningitis and hydrocephalus in an HTLV-1 carrier with increased proviral load. J Infect Chemother 9 :355–357.

    • Search Google Scholar
    • Export Citation
  • 5

    Neva FA, Oliveira J, Gam AA, 1998. Interferon-γ and interleukin-4 responses in relation to serum IgE levels in persons infected with human T lymphotropic virus type I and Strongyloides stercoralis. J Infect Dis 178 :1856–1859.

    • Search Google Scholar
    • Export Citation
  • 6

    Porto MAF, Neva FA, Lisboa W, Thompson R, Alcântara L, Carvalho EM, 2001. HTLV-1 decreases Th2 type of immune response in patients with strongyloidiasis. Parasite Immunol 23 :503–507.

    • Search Google Scholar
    • Export Citation
  • 7

    Porto MAF, Oliveira Filho J, Neva FA, Orge G, Alcântara L, Gam A, Carvalho EM, 2001. Influence of HTLV-1 infection on serologic and skin tests for strongyloidiasis. Am J Trop Med Hyg 65 :610–613.

    • Search Google Scholar
    • Export Citation
  • 8

    Morimoto J, Kaneoka H, Sasatomi Y, Sato YN, Murata T, Ogahara S, Sakata N, 2002. Disseminated strongyloidiasis in nephrotic syndrome. Clin Nephrol 57 :398–401.

    • Search Google Scholar
    • Export Citation
  • 9

    Lemos LB, Qu Z, Laucirica R, Fred HL, 2003. Hyperinfection syndrome in strongyloidiasis: report of two cases. Ann Diagn Pathol 7 :87–94.

    • Search Google Scholar
    • Export Citation
  • 10

    O’Doherty MJ, van de Pette JE, Nunan TO, Croft DN, 1984. Recurrent Strongyloides stercoralis infection in a patient with T-cell lymphoma-leukaemia. Lancet 1 :858.

    • Search Google Scholar
    • Export Citation
  • 11

    Phelps KR, Ginsberg SS, Cinningham AW, Tschachler E, Dosik H, 1991. Case report: adult T-cell leukemia/lymphoma associated with recurrent Strongyloides hyperinfection. Am J Med Sci 302 :224–228.

    • Search Google Scholar
    • Export Citation
  • 12

    Patey O, Gessain A, Breuil J, Courillon-Mallet A, Daniel MT, Miclea JM, Roucayrol AM, Sigaux F, Lafaix C, 1992. Seven years of recurrent severe strongyloidiasis in an HTLV-I-infected man who developed adult T-cell leukaemia. AIDS 6 :575–579.

    • Search Google Scholar
    • Export Citation
  • 13

    Satoh M, Toma H, Sato Y, Takara M, Shiroma Y, Kiyuna S, Hirayama K, 2002. Reduced efficacy of treatment of strongyloidiasis in HTLV-1 carriers related to enhanced expression of IFN-γ and TGF-β1. Clin Exp Immunol 127 :354–359.

    • Search Google Scholar
    • Export Citation

Author Notes

Reprint requests: Edgar M. Carvalho, Serviço de Imunologia, Hospital Universitário Professor Edgard Santos, 5° andar, Rua João das Botas, s/n Canela 40110-160, Salvador, Bahia, Brazil, Telephone: 55-71-237-7353, Fax: 55-71-245-7110, E-mail: edgar@ufba.br.
Save