• 1

    Carvalho EM, Porto A, 2004. Epidemiological and clinical interaction between HTLV-1 and Strongyloides stercoralis. Parasite Immunol 26 :487–497.

    • Search Google Scholar
    • Export Citation
  • 2

    Hirata T, Uchima N, Kishimoto K, Zaha O, Kinjo N, Hokama A, Sakugawa H, Kinjo F, Fujita J, 2006. Impairment of host immune response against Strongyloides stercoralis by human T cell lymphotropic virus type 1 infection. Am J Trop Med Hyg 74 :246–249.

    • Search Google Scholar
    • Export Citation
  • 3

    Arakaki T, Iwanaga M, Kinjo F, Saito A, Asato R, Ikeshiro T, 1990. Efficacy of agar-plate culture in detection of Strongyloides stercoralis infection. J Parasitol 76 :425–428.

    • Search Google Scholar
    • Export Citation
  • 4

    Zaha O, Hirata T, Kinjo F, Saito A, 2000. Strongyloidiasis-progress in diagnosis and treatment. Intern Med 39 :695–700.

  • 5

    Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H, 1991. A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg 45 :518–521.

    • Search Google Scholar
    • Export Citation
  • 6

    Uparanukraw P, Phongsri S, Morakote N, 1999. Fluctuations of larval excretion in Strongyloides stercoralis infection. Am J Trop Med Hyg 60 :967–973.

    • Search Google Scholar
    • Export Citation
  • 7

    Sato Y, Kobayashi J, Toma H, Shiroma Y, 1995. Efficacy of stool examination for detection of Strongyloides infection. Am J Trop Med Hyg 53 :248–250.

    • Search Google Scholar
    • Export Citation
  • 8

    Moustafa MA, 1997. An evaluation of the modified agar plate method for diagnosis of Strongyloides stercoralis. J Egypt Soc Parasitol 27 :571–579.

    • Search Google Scholar
    • Export Citation
  • 9

    Siddiqui AA, Berk SL, 2001. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 33 :1040–1047.

  • 10

    Groove DI, 1989. Strongyloidiasis: A Major Roundworm Infection of Man. New York: Taylor & Francis.

  • 11

    Garcia LS, 2007. Diagnostic Medical Parasitology. Fifth edition. Washington, DC: ASM Press.

    • Crossref
    • Export Citation
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Increased Detection Rate of Strongyloides stercoralis by Repeated Stool Examinations Using the Agar Plate Culture Method

Tetsuo HirataDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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Hiroshi NakamuraDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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Nagisa KinjoDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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Akira HokamaDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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Fukunori KinjoDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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Nobuhisa YamaneDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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Jiro FujitaDepartment of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan; Department of Clinical Laboratories, Ryukyu University Hospital, Okinawa, Japan; Department of Endoscopy, Ryukyu University Hospital, Okinawa, Japan

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To clarify the efficacy of repeated stool examinations by the agar plate culture method for the detection of Strongyloides stercoralis infection, 4,071 stool samples collected from 2,406 patients > 50 years of age in Ryukyu University Hospital were examined. The cumulative detection rate of S. stercoralis infection was 4.7% (112/2,406). At the first, second, third, and beyond fourth examinations, the detection rates were 3.6% (86/2,406), 1.5% (12/786), 2.6% (10/392), and 2.0% (4/198), respectively. From these results, the cumulative detection rate was estimated to be 7.4% when three stool samples were examined for all patients. Our study showed that repeated stool examinations increase the sensitivity of detection of S. stercoralis infection.

Strongyloidiasis is widely distributed in tropical and subtropical regions, and it is estimated that 50–100 million individuals worldwide are infected with Strongyloides stercoralis.1 Okinawa prefecture, a subtropical region of Japan, is known as an endemic area for this infection. In an earlier study in Okinawa, we found that the prevalence rate of S. stercoralis infection was 6.3% and that > 95% of the infected patients were > 50 years of age.2 The infective larvae of S. stercoralis develops in soil and penetrates intact skin. After infection, the larvae migrate to the duodenum and grow into mature females. Rhabditiform larvae hatched from eggs are ejected from the host. However, some of them develop into filariform larvae and reinfect through the colon or anal skin (autoinfection). Therefore, once a person is infected by S. stercoralis, the infection can last for a long time.

It has been reported that the agar plate culture method is highly efficient for the detection of S. stercoralis infection35 and that repeated stool examinations would increase the cumulative detection of S. stercoralis infection.611 However, there have been no large-scale studies regarding the association between the detection rate of S. stercoralis infection and repeated stool examinations using the agar plate culture method in previously unproven cases.

This study included 2,406 patients > 50 years of age in Ryukyu University Hospital, Okinawa, Japan, between 2004 and 2006. Patients previously diagnosed with strongyloidiasis were excluded from the study. The subjects consisted of 1,337 men and 1,069 women, with a mean age (SD) of 67.1 (10.0) years. A total of 4,071 stool samples collected from the 2,406 patients were examined for the detection of S. stercoralis infection using the agar plate culture method. The total detection rate of S. stercoralis infection was 4.7% (112/2,406). In all the S. stercoralis–positive patients, the severity of the strongyloidiasis was mild. The detection rates of S. stercoralis infection in men and women were 5.8% (78/1,337) and 3.2% (34/ 1,069), respectively, and significantly higher in men than in women (P = 0.002, χ2 test). At the first examination, the detection rate of S. stercoralis infection was 3.6% (86/2,406). In 786 of 2,320 patients negative for S. stercoralis infection at the first examination, the stool examination was repeated, and 1.5% (12/786) of the patients were converted to positive for S. stercoralis infection. In 392 of 774 patients negative for S. stercoralis infection at the second examination, the stool examination was repeated again, and 2.6% (10/392) of the patients were converted to positive for S. stercoralis infection (Table 1). From these results, the cumulative detection rate was estimated to 7.4% when three stool samples were examined by the agar plate culture method for all patients. The estimated detection rate after examination of three stool samples was ~2-fold higher than that after a single examination.

Our results showed that repeated stool examinations increase the sensitivity of detection of S. stercoralis. Uparanukraw and others6 previously reported that the agar plate culture method detected S. stercoralis infection in 87.5%–96.4% of S. stercoralis–proven cases in a single examination, and 0%–5.9% of S. stercoralis–negative cases in a single examination. Sato and others7 showed that the agar plate culture method detected 57.8% of proven cases in a single examination. However, when three stool specimens were examined, their cumulative detection rate increased to 84.8%. Moustafa8 reported that the agar plate culture method detected 70.3% and 96.2% of S. stercoralis–proven cases by 1- and 3-day examinations, respectively. It is well known that detection of S. stercoralis larvae in feces is difficult, unless the patients have severe strongyloidiasis.9 This is because of the low output of S. stercoralis larvae in the stools of patients with chronic low-level infection.

In summary, this study showed that repeated stool examinations can increase the detection rate of S. stercoralis infection in previously unproven cases. In patients with mild strongyloidiasis, the estimated cumulative detection rate after examination of three stool samples was ~2-fold higher than that after a single examination.

Table 1

Association between S. stercoralis detection rates and numbers of stool examinations by the agar plate culture method

No. of stool examinations Detection rates of S. stercoralis* Cumulative detection rates of S. stercoralis* Estimated no. of patients positive for S. stercoralis after examination of stool samples for all patients Estimated cumulative detection rates of S. stercoralis after examination of stool samples for all patients*
* Percent (no. of S. stercoralis–positive patients/no. of patients examined).
† “Detection rate” multiplied by “no. of patients negative for S. stercoralis infection at the first examination.”
‡ “Detection rate” multiplied by “no. of patients negative for S. stercoralis infection at the first and second examinations.”
1 3.6 (86/2,406) 3.6 (86/2,406) 86 3.6 (86/2,406)
2 1.5 (12/786) 4.1 (98/2,406) 35† 5.0 (121/2,406)
3 2.6 (10/392) 4.5 (108/2,406) 58‡ 7.4 (178/2,406)
≥4 2.0 (4/198) 4.7 (112/2,406)

*

Address correspondence to Tetsuo Hirata, 207 Uehara, Nishihara 905-0125, Japan. E-mail: h400314@med.u-ryukyu.ac.jp

Authors’ addresses: Tetsuo Hirata, Akira Hokama, and Jiro Fujita, Department of Medicine and Therapeutics, Control and Prevention of Infectious Diseases, Faculty of Medicine, University of the Ryukyus, 207 Uehara, Nishihara, Okinawa, Japan, Telephone: 81-98-895-1144, Fax: 81-98-895-1414, E-mails: h400314@med.u-ryukyu.ac.jp, hokama-a@med.u-ryukyu.ac.jp, and fujita@med.u-ryukyu.ac.jp. Hiroshi Nakamura and Nobuhisa Yamane, Department of Clinical Laboratories, Ryukyu University Hospital, 207 Uehara, Nishihara, Okinawa, Japan, Telephone: 81-98-895-1319, Fax: 81-98-895-1453, E-mails: nakahiro@jim.u-ryukyu.ac.jp and nobie@med.u-ryukyu.ac.jp. Nagisa Kinjo and Fukunori Kinjo, Department of Endos-copy, Ryukyu University Hospital, 207 Uehara, Nishihara, Okinawa, Japan, Telephone: 81-98-895-1144, Fax: 81-98-895-1414, E-mails: nagisa-k@med.u-ryukyu.ac.jp and kinjofuk@med.u-ryukyu.ac.jp.

REFERENCES

  • 1

    Carvalho EM, Porto A, 2004. Epidemiological and clinical interaction between HTLV-1 and Strongyloides stercoralis. Parasite Immunol 26 :487–497.

    • Search Google Scholar
    • Export Citation
  • 2

    Hirata T, Uchima N, Kishimoto K, Zaha O, Kinjo N, Hokama A, Sakugawa H, Kinjo F, Fujita J, 2006. Impairment of host immune response against Strongyloides stercoralis by human T cell lymphotropic virus type 1 infection. Am J Trop Med Hyg 74 :246–249.

    • Search Google Scholar
    • Export Citation
  • 3

    Arakaki T, Iwanaga M, Kinjo F, Saito A, Asato R, Ikeshiro T, 1990. Efficacy of agar-plate culture in detection of Strongyloides stercoralis infection. J Parasitol 76 :425–428.

    • Search Google Scholar
    • Export Citation
  • 4

    Zaha O, Hirata T, Kinjo F, Saito A, 2000. Strongyloidiasis-progress in diagnosis and treatment. Intern Med 39 :695–700.

  • 5

    Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H, 1991. A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg 45 :518–521.

    • Search Google Scholar
    • Export Citation
  • 6

    Uparanukraw P, Phongsri S, Morakote N, 1999. Fluctuations of larval excretion in Strongyloides stercoralis infection. Am J Trop Med Hyg 60 :967–973.

    • Search Google Scholar
    • Export Citation
  • 7

    Sato Y, Kobayashi J, Toma H, Shiroma Y, 1995. Efficacy of stool examination for detection of Strongyloides infection. Am J Trop Med Hyg 53 :248–250.

    • Search Google Scholar
    • Export Citation
  • 8

    Moustafa MA, 1997. An evaluation of the modified agar plate method for diagnosis of Strongyloides stercoralis. J Egypt Soc Parasitol 27 :571–579.

    • Search Google Scholar
    • Export Citation
  • 9

    Siddiqui AA, Berk SL, 2001. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 33 :1040–1047.

  • 10

    Groove DI, 1989. Strongyloidiasis: A Major Roundworm Infection of Man. New York: Taylor & Francis.

  • 11

    Garcia LS, 2007. Diagnostic Medical Parasitology. Fifth edition. Washington, DC: ASM Press.

    • Crossref
    • Export Citation
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