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Tropical pyomyositis and human toxocariasis: a clinical and experimental study
BRIEF OBSERVATIONS
Tropical Pyomyositis and Human Toxocariasis: A Clinical and Experimental Study
enzyme-linked immunosorbent assay (ELISA; Syntron Bioresearch Inc., Carlsbad, California); serologic tests for toxocariasis were performed by ELISA (8,9). The study was approved by the ethics committee of the Faculty of Medicine, Federal University of Minas Gerais, Brazil, and informed consent was obtained from patients and controls.
Abdunnabi A. Rayes, MD, PhD, Vandack Nobre, MD, MSc, Daniela M. Teixeira, MD, J. C. Serufo, MD, PhD, Geraldo Brasileiro Filho, MD, PhD, Carlos M. Antunes, PhD, J. R. Lambertucci, MD, PhD
Studies in Animals
I
Infection with Toxocara canis larvae usually occurs through the ingestion of contaminated rabbit, pork, beef, or chicken (1,2). In children, pica is a common source of infection. Pyomyositis is a bacterial infection of the skeletal muscles. Most cases occur in the tropics, hence the term tropical pyomyositis (3,4). In the United States, the disease is very uncommon, occurring mostly in patients who have recently immigrated from the tropics. The presumed pathogenesis of pyomyositis involves a prior bacteremia with Staphylococcus aureus, which is responsible for 95% of the cases in tropical areas and 75% of the cases in North America. As yet, there is no convincing evidence that relates pyomyositis to predisposing circumstances that are peculiar to the tropics, such as malaria, filariasis, or arbovirus infection. We present clinical and experimental data about the association between T. canis infection and tropical pyomyositis caused by S. aureus (5–7).
MATERIAL AND METHODS Studies in Humans Between March 1995 and March 1998, we prospectively studied 20 patients with tropical pyomyositis who were admitted to five hospitals in Belo Horizonte, Brazil, and who were referred to us for treatment. Patients were included if they met at least two of the following criteria: a clinical picture consistent with tropical pyomyositis (eg, distinct muscle tenderness and swelling in a febrile patient); confirmation with ultrasound or computerized tomography; and a culture of the abscess when it was drained. We enrolled a control group of 20 patients matched by age (⫾ 2 years) and sex who were admitted to the same hospitals. Demographic characteristics of the control group were similar to those of the study group. The controls were admitted for the treatment of diabetes mellitus, pneumonia, cirrhosis, Schistosoma mansoni infection, asthma, influenza, fever of undetermined origin, or pulmonary tuberculosis. Serum total immunoglobulin E (IgE) levels were measured in both groups using an 422
䉷2000 by Excerpta Medica, Inc. All rights reserved.
Fifty-eight Swiss mice, weighing 25 g to 30 g, were divided into four groups: 29 mice were infected with 1,000 embryonated eggs of T. canis at day 0 and weekly with S. aureus; 13 mice were infected with only S. aureus; 6 mice were infected with only 1,000 infective eggs of T. canis at day 0; and 10 mice served as a control group without any infection. Infection with larva was undertaken according to the technique of Abo-Shehada et al (10). For infection with S. aureus, bacteria were isolated from patients admitted to the hospital with staphylococcal infections; mice were injected via a caudal vein. The number of bacteria varied from 0.8 ⫻ 106 to 4 ⫻ 106 units per infection. Mice were observed daily and were killed when they became ill, or examined postmortem when they died. The carcasses were carefully examined for the presence of muscle abscesses. Specimens were taken from areas with abscess and from apparently normal muscles and were kept in 10% formalin until processed for standard histologic study. Statistical methods included McNemar’s test (matched design) to compare whether serologic tests for toxocariasis were positive in patients and controls. Serum IgE levels were compared using a paired t test. The chi-square test was used to compare the proportions with abscesses among the mice.
RESULTS Seventeen (85%) of the 20 patients were men and 8 of them were 16 years old or younger. All had fever; most had painful swelling of one or more muscles (Table 1). Fifteen patients reported a previous history of pyoderma. Culture of the abscesses was positive in 16 (94%) of 17 patients examined. In 14, S. aureus resistant only to penicillin and ampicillin was isolated. Blood cultures were positive for S. aureus in only 2 of 16 patients. Surgical exploration in 2 patients did not reveal a distinct muscle abscess, but pyomyositis was confirmed by muscle biopsy; in both patients, a possible fluid collection was suggested by ultrasound. Serology for toxocariasis was positive in 8 (40%) of the 20 patients and in 1(5%) of the 20 controls (P ⫽ 0.008). Serum IgE levels were not significantly different in patients and controls. Stool examination for parasites was positive in 5 pa0002-9343/00/$–see front matter PII S0002-9343(00)00512-X
Tropical Pyomyositis and Human Toxocariasis/Rayes et al
Table 1. Signs and Symptoms in 20 Patients with Tropical Pyomyositis Number (Percent) Symptoms Fever Painful swelling Chills Trauma Signs Fever Inflammatory signs* Involvement of ⬎1 muscle Regional lymphadenopathy
20 (100) 16 (80) 13 (65) 2 (10) 20 (100) 13 (65) 10 (50) 2 (10)
* Heat, redness, and swelling.
tients: Ascaris lumbricoides in 2 and Ancylostoma duodenale, Hymenolepis nana, and Schistosoma mansoni in 1 each. Patients were treated either with antibiotics alone (4 [20%]), antibiotics and percutaneous drainage (4 [20%]), or antibiotics and open surgery (12 [60%]). All patients recovered from the acute illness and were discharged from the hospital with minor sequelae (eg, scars). In the experimental study, muscle abscesses were more frequently observed in mice infected with T. canis and S. aureus (Table 2, P ⬍0.01). S. aureus was isolated from the abscesses of 3 mice. On microscopic examination, a constant feature was the presence of a collection of purulent necrotic material, often associated with colonies of bacteria (Figure 1). Larvae were observed in sections of the affected muscles, which were surrounded by an inflammatory infiltrate (Figure 2).
DISCUSSION We found an association between toxocariasis and pyogenic abscesses of skeletal muscle. We do not know the Table 2. Development of Muscle Abscesses in Mice Infected with Toxocara canis, Staphylococcus aureus, or Both, Compared with Controls
Group Toxocara canis and Staphylococcus aureus S. aureus alone T. canis alone Not infected
Number of Mice
Number of Mice with Muscle Abscess (Percent)
29
14 (48)*
13 6 10
1 (08)* 0 0
* P ⫽ 0.001 compared with the other three groups.
exact mechanisms involved in this association. Some patients reported recurrent pyoderma, either as a result of poor socioeconomic conditions, or possibly as a manifestation of altered immune function due to T. canis infections, which may be the foci for bacteremia and more severe infections like muscle abscess. The greater prevalence of positive serologic tests for toxocariasis among patients compared with controls suggests that toxocariasis is a predisposing factor for the development of pyogenic muscle abscess. In a study of 65 patients with tropical pyomyositis in Africa, O’Brien (11) reported finding a larva from an unknown species in the abscess of 1 patient. O’Brien divided the clinical course of tropical pyomyositis into three stages. In the first stage, the patient presents with local pain and a woody sensation in the involved muscle without inflammatory signs. This stage is attributed to the invasion of the muscle with the larvae, causing a transitory myositis that may resolve spontaneously. At this stage, surgical exploration of the muscle does not reveal an abscess, although a mass lesion can be revealed by imaging techniques, as was observed in 2 of our patients. In the second stage, there are constitutional symptoms and local inflammatory signs. Surgical exploration of the affected muscle may reveal a large collection of pus. In the third stage, there is a granulomatous mass with central caseation. In humans, T. canis larvae migrate through the tissues of many organs, such as the liver, lungs, brain, eyes, kidneys, muscles, and spinal cord (12). They frequently induce the formation of granuloma that can be the site of bacterial colonization, especially with S. aureus. The structure of the granuloma varies with its age (13). In the later stages of its development the granuloma contains collagen, to which S. aureus can bind (14). Systemically, toxocariasis causes activation of TH2 cells, leading to the production of interleukin-4 and interleukin-5. These alterations lead to defective neutrophil chemotaxis and decreased ability of macrophages to destroy intracellular pathogens (15,16). Caldwell et al (17) reported defective neutrophil function in a patient with toxocariasis that normalized after treatment with diethylcarbamazine. Tropical pyomyositis has also been described in patients with the acquired immunodeficiency syndrome (AIDS) (18). It is possible that in AIDS patients, defective immunity may lead to larval reactivation, followed by the development of abscesses. The availability of better techniques for the diagnosis of toxocariasis, together with the presence of more effective treatment measures, should encourage physicians to consider the diagnosis of toxocariasis. If diagnosed, it should be treated to avoid possible complications. We believe that infection with T. canis is a cofactor in the development of tropical pyomyositis. If serologic tests for
October 1, 2000
THE AMERICAN JOURNAL OF MEDICINE威
Volume 109 423
Tropical Pyomyositis and Human Toxocariasis/Rayes et al
Figure 1. Muscle abscess (thin arrow) with a collection of bacteria (thick arrow; hematoxylin and eosin stain, ⫻180).
Figure 2. An inflammatory infiltrate around a larva (arrow) in the skeletal muscle of a mouse infected with Toxocara canis (immunohistochemical stain, ⫻400). 424
October 1, 2000
THE AMERICAN JOURNAL OF MEDICINE威
Volume 109
Tropical Pyomyositis and Human Toxocariasis/Rayes et al
T. canis infection are positive, treatment for toxocariasis, using albendazole or ivermectin (19,20) should be considered.
11. 12.
ACKNOWLEDGMENT We wish to thank Dr. Fausto E. L. Pereira (Faculty of Medicine, Federal University of Espirito Santo) for his help with the immunohistochemical study and Drs. Walter dos Santos Lima and Mucio F. B. Ribeiro (ICB-UFMG) for their assistance during the experimental work.
13. 14.
15.
REFERENCES 1. Beaver PC, Snyder CH, Carrera GM, et al. Chronic eosinophilia due to visceral larva migrans: report of three cases. J Pediatr. 1952;9:7– 19. 2. Sturchler D, Weiss N, Gassner M. Transmission of toxocariasis. J Infect Dis. 1990;162:571. 3. Chiedozi LC. Pyomyositis. Review of 205 cases in 112 patients. Am J Surg. 1979;137:255–259. 4. Shepherd JJ. Tropical myositis: is it an entity and what is its cause? Lancet. 1983:1240 –1242. 5. Lambertucci JR, Rayes A, Serufo JC, et al. Visceral larva migrans and tropical pyomyositis: a case report. Rev Inst Med Trop Sa˜o Paulo. 1998;40:383–385. 6. Rayes AA, Lambertucci, JR. Visceral larva migrans and pyogenic liver abscess. Am J Gastroenterol. 1999;94:1116. 7. Rayes AA, Teixeira DM, Nobre V, et al. Visceral larva migrans syndrome complicated by liver abscess: a case report. Scand J Infect Dis. 1999;31:324 –325. 8. Glickman L, Schantz P, Dombroske R, Cypess R. Evaluation of serodiagnostic tests for visceral larva migrans. Am J Trop Med Hyg. 1978;27:92–98. 9. Camargo ED, Nakamura PM, Vaz AJ, et al. Standardization of DotELISA for the serological diagnosis of toxocariasis and comparison of the assay with ELISA. Rev Inst Med Trop Sa˜o Paulo. 1992;34:55– 60. 10. Abo-Shehada MN, Al-Zubaidy BAM, Herbert IV. The migration of
16.
17.
18.
19.
20.
larval Toxocara canis in mice. I. Migration through the intestine in primary infections. Vet Parasitol. 1984;17:65–73. O’Brien DD. Tropical pyomyositis. A manifestation of larva migrans? J R Army Med Corps. 1963;109:43–50. Margareth HD, Smith MD, Beaver PC. Persistence and distribution of toxocara larvae in the tissues of children and mice. Pediatrics. 1953;12:491– 496. Kayes SG, Oaks JA. Development of the granulomatous response in murine toxocariasis. Initial events. Am J Pathol. 1978;93:277–285. McGavin MHD, Krajewska-Pietrasik D, Ryde´n C, Hook M. Identification of a Staphylococcus aureus extracellular matrix-binding protein with broad specificity. Infect Immun. 1993;61:2479 –2485. Del Prete GF, De Carli M, Mastromauro C, et al. Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand in vitro human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production. J Clin Invest. 1991;88:346 –350. Lambertucci JR. Hyperimmunoglobulinemia E, parasitic diseases, and staphylococcal infection. Rev Soc Bras Med Trop. 1996;29:407– 410. Caldwell K, Lobell M, Coccia PF. Mitogenic response to Toxocara antigen and chemotactic defect in visceral larva migrans. Am J Dis Child. 1980;134:845– 847. Ansaloni L, Re MC. High HIV seroprevalence among patients with pyomyositis in Northern Uganda. Trop Med Int Health. 1996;1: 210 –212. Sturchler D, Schubarth P, Gualzata TA, et al. Thiabendazol versus albendazol in treatment of toxocariasis: a clinical trial. Ann Trop Med Parasitol. 1989;83:473– 478. Konate A, Duhamel O, Basset D, et al. Toxocarose et troubles fonctionnels intestinaux. Presentation de 4 cas. Gastroenterol Clin Biol. 1996;20:909 –911.
From the Departments of Internal Medicine (AAR, VN, DMT, JCS, JRL) and Clinical Pathology (GBF), School of Medicine, and the Department of Epidemiology (CMA), Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, Brazil. Correspondence should be addressed to J. R. Lambertucci, MD, PhD, Departamento de Clı´nica Medica, Faculdade de Medicina da UFMG, Av. Alfredo Balena 190, CEP: 30130-100, Belo Horizonte-MG, Brazil. Manuscript submitted January 10, 2000, and accepted in revised form May 31, 2000.
October 1, 2000
THE AMERICAN JOURNAL OF MEDICINE威
Volume 109 425
Tropical Pyomyositis and Human Toxocariasis: A Clinical and Experimental Study
enzyme-linked immunosorbent assay (ELISA; Syntron Bioresearch Inc., Carlsbad, California); serologic tests for toxocariasis were performed by ELISA (8,9). The study was approved by the ethics committee of the Faculty of Medicine, Federal University of Minas Gerais, Brazil, and informed consent was obtained from patients and controls.
Abdunnabi A. Rayes, MD, PhD, Vandack Nobre, MD, MSc, Daniela M. Teixeira, MD, J. C. Serufo, MD, PhD, Geraldo Brasileiro Filho, MD, PhD, Carlos M. Antunes, PhD, J. R. Lambertucci, MD, PhD
Studies in Animals
I
Infection with Toxocara canis larvae usually occurs through the ingestion of contaminated rabbit, pork, beef, or chicken (1,2). In children, pica is a common source of infection. Pyomyositis is a bacterial infection of the skeletal muscles. Most cases occur in the tropics, hence the term tropical pyomyositis (3,4). In the United States, the disease is very uncommon, occurring mostly in patients who have recently immigrated from the tropics. The presumed pathogenesis of pyomyositis involves a prior bacteremia with Staphylococcus aureus, which is responsible for 95% of the cases in tropical areas and 75% of the cases in North America. As yet, there is no convincing evidence that relates pyomyositis to predisposing circumstances that are peculiar to the tropics, such as malaria, filariasis, or arbovirus infection. We present clinical and experimental data about the association between T. canis infection and tropical pyomyositis caused by S. aureus (5–7).
MATERIAL AND METHODS Studies in Humans Between March 1995 and March 1998, we prospectively studied 20 patients with tropical pyomyositis who were admitted to five hospitals in Belo Horizonte, Brazil, and who were referred to us for treatment. Patients were included if they met at least two of the following criteria: a clinical picture consistent with tropical pyomyositis (eg, distinct muscle tenderness and swelling in a febrile patient); confirmation with ultrasound or computerized tomography; and a culture of the abscess when it was drained. We enrolled a control group of 20 patients matched by age (⫾ 2 years) and sex who were admitted to the same hospitals. Demographic characteristics of the control group were similar to those of the study group. The controls were admitted for the treatment of diabetes mellitus, pneumonia, cirrhosis, Schistosoma mansoni infection, asthma, influenza, fever of undetermined origin, or pulmonary tuberculosis. Serum total immunoglobulin E (IgE) levels were measured in both groups using an 422
䉷2000 by Excerpta Medica, Inc. All rights reserved.
Fifty-eight Swiss mice, weighing 25 g to 30 g, were divided into four groups: 29 mice were infected with 1,000 embryonated eggs of T. canis at day 0 and weekly with S. aureus; 13 mice were infected with only S. aureus; 6 mice were infected with only 1,000 infective eggs of T. canis at day 0; and 10 mice served as a control group without any infection. Infection with larva was undertaken according to the technique of Abo-Shehada et al (10). For infection with S. aureus, bacteria were isolated from patients admitted to the hospital with staphylococcal infections; mice were injected via a caudal vein. The number of bacteria varied from 0.8 ⫻ 106 to 4 ⫻ 106 units per infection. Mice were observed daily and were killed when they became ill, or examined postmortem when they died. The carcasses were carefully examined for the presence of muscle abscesses. Specimens were taken from areas with abscess and from apparently normal muscles and were kept in 10% formalin until processed for standard histologic study. Statistical methods included McNemar’s test (matched design) to compare whether serologic tests for toxocariasis were positive in patients and controls. Serum IgE levels were compared using a paired t test. The chi-square test was used to compare the proportions with abscesses among the mice.
RESULTS Seventeen (85%) of the 20 patients were men and 8 of them were 16 years old or younger. All had fever; most had painful swelling of one or more muscles (Table 1). Fifteen patients reported a previous history of pyoderma. Culture of the abscesses was positive in 16 (94%) of 17 patients examined. In 14, S. aureus resistant only to penicillin and ampicillin was isolated. Blood cultures were positive for S. aureus in only 2 of 16 patients. Surgical exploration in 2 patients did not reveal a distinct muscle abscess, but pyomyositis was confirmed by muscle biopsy; in both patients, a possible fluid collection was suggested by ultrasound. Serology for toxocariasis was positive in 8 (40%) of the 20 patients and in 1(5%) of the 20 controls (P ⫽ 0.008). Serum IgE levels were not significantly different in patients and controls. Stool examination for parasites was positive in 5 pa0002-9343/00/$–see front matter PII S0002-9343(00)00512-X
Tropical Pyomyositis and Human Toxocariasis/Rayes et al
Table 1. Signs and Symptoms in 20 Patients with Tropical Pyomyositis Number (Percent) Symptoms Fever Painful swelling Chills Trauma Signs Fever Inflammatory signs* Involvement of ⬎1 muscle Regional lymphadenopathy
20 (100) 16 (80) 13 (65) 2 (10) 20 (100) 13 (65) 10 (50) 2 (10)
* Heat, redness, and swelling.
tients: Ascaris lumbricoides in 2 and Ancylostoma duodenale, Hymenolepis nana, and Schistosoma mansoni in 1 each. Patients were treated either with antibiotics alone (4 [20%]), antibiotics and percutaneous drainage (4 [20%]), or antibiotics and open surgery (12 [60%]). All patients recovered from the acute illness and were discharged from the hospital with minor sequelae (eg, scars). In the experimental study, muscle abscesses were more frequently observed in mice infected with T. canis and S. aureus (Table 2, P ⬍0.01). S. aureus was isolated from the abscesses of 3 mice. On microscopic examination, a constant feature was the presence of a collection of purulent necrotic material, often associated with colonies of bacteria (Figure 1). Larvae were observed in sections of the affected muscles, which were surrounded by an inflammatory infiltrate (Figure 2).
DISCUSSION We found an association between toxocariasis and pyogenic abscesses of skeletal muscle. We do not know the Table 2. Development of Muscle Abscesses in Mice Infected with Toxocara canis, Staphylococcus aureus, or Both, Compared with Controls
Group Toxocara canis and Staphylococcus aureus S. aureus alone T. canis alone Not infected
Number of Mice
Number of Mice with Muscle Abscess (Percent)
29
14 (48)*
13 6 10
1 (08)* 0 0
* P ⫽ 0.001 compared with the other three groups.
exact mechanisms involved in this association. Some patients reported recurrent pyoderma, either as a result of poor socioeconomic conditions, or possibly as a manifestation of altered immune function due to T. canis infections, which may be the foci for bacteremia and more severe infections like muscle abscess. The greater prevalence of positive serologic tests for toxocariasis among patients compared with controls suggests that toxocariasis is a predisposing factor for the development of pyogenic muscle abscess. In a study of 65 patients with tropical pyomyositis in Africa, O’Brien (11) reported finding a larva from an unknown species in the abscess of 1 patient. O’Brien divided the clinical course of tropical pyomyositis into three stages. In the first stage, the patient presents with local pain and a woody sensation in the involved muscle without inflammatory signs. This stage is attributed to the invasion of the muscle with the larvae, causing a transitory myositis that may resolve spontaneously. At this stage, surgical exploration of the muscle does not reveal an abscess, although a mass lesion can be revealed by imaging techniques, as was observed in 2 of our patients. In the second stage, there are constitutional symptoms and local inflammatory signs. Surgical exploration of the affected muscle may reveal a large collection of pus. In the third stage, there is a granulomatous mass with central caseation. In humans, T. canis larvae migrate through the tissues of many organs, such as the liver, lungs, brain, eyes, kidneys, muscles, and spinal cord (12). They frequently induce the formation of granuloma that can be the site of bacterial colonization, especially with S. aureus. The structure of the granuloma varies with its age (13). In the later stages of its development the granuloma contains collagen, to which S. aureus can bind (14). Systemically, toxocariasis causes activation of TH2 cells, leading to the production of interleukin-4 and interleukin-5. These alterations lead to defective neutrophil chemotaxis and decreased ability of macrophages to destroy intracellular pathogens (15,16). Caldwell et al (17) reported defective neutrophil function in a patient with toxocariasis that normalized after treatment with diethylcarbamazine. Tropical pyomyositis has also been described in patients with the acquired immunodeficiency syndrome (AIDS) (18). It is possible that in AIDS patients, defective immunity may lead to larval reactivation, followed by the development of abscesses. The availability of better techniques for the diagnosis of toxocariasis, together with the presence of more effective treatment measures, should encourage physicians to consider the diagnosis of toxocariasis. If diagnosed, it should be treated to avoid possible complications. We believe that infection with T. canis is a cofactor in the development of tropical pyomyositis. If serologic tests for
October 1, 2000
THE AMERICAN JOURNAL OF MEDICINE威
Volume 109 423
Tropical Pyomyositis and Human Toxocariasis/Rayes et al
Figure 1. Muscle abscess (thin arrow) with a collection of bacteria (thick arrow; hematoxylin and eosin stain, ⫻180).
Figure 2. An inflammatory infiltrate around a larva (arrow) in the skeletal muscle of a mouse infected with Toxocara canis (immunohistochemical stain, ⫻400). 424
October 1, 2000
THE AMERICAN JOURNAL OF MEDICINE威
Volume 109
Tropical Pyomyositis and Human Toxocariasis/Rayes et al
T. canis infection are positive, treatment for toxocariasis, using albendazole or ivermectin (19,20) should be considered.
11. 12.
ACKNOWLEDGMENT We wish to thank Dr. Fausto E. L. Pereira (Faculty of Medicine, Federal University of Espirito Santo) for his help with the immunohistochemical study and Drs. Walter dos Santos Lima and Mucio F. B. Ribeiro (ICB-UFMG) for their assistance during the experimental work.
13. 14.
15.
REFERENCES 1. Beaver PC, Snyder CH, Carrera GM, et al. Chronic eosinophilia due to visceral larva migrans: report of three cases. J Pediatr. 1952;9:7– 19. 2. Sturchler D, Weiss N, Gassner M. Transmission of toxocariasis. J Infect Dis. 1990;162:571. 3. Chiedozi LC. Pyomyositis. Review of 205 cases in 112 patients. Am J Surg. 1979;137:255–259. 4. Shepherd JJ. Tropical myositis: is it an entity and what is its cause? Lancet. 1983:1240 –1242. 5. Lambertucci JR, Rayes A, Serufo JC, et al. Visceral larva migrans and tropical pyomyositis: a case report. Rev Inst Med Trop Sa˜o Paulo. 1998;40:383–385. 6. Rayes AA, Lambertucci, JR. Visceral larva migrans and pyogenic liver abscess. Am J Gastroenterol. 1999;94:1116. 7. Rayes AA, Teixeira DM, Nobre V, et al. Visceral larva migrans syndrome complicated by liver abscess: a case report. Scand J Infect Dis. 1999;31:324 –325. 8. Glickman L, Schantz P, Dombroske R, Cypess R. Evaluation of serodiagnostic tests for visceral larva migrans. Am J Trop Med Hyg. 1978;27:92–98. 9. Camargo ED, Nakamura PM, Vaz AJ, et al. Standardization of DotELISA for the serological diagnosis of toxocariasis and comparison of the assay with ELISA. Rev Inst Med Trop Sa˜o Paulo. 1992;34:55– 60. 10. Abo-Shehada MN, Al-Zubaidy BAM, Herbert IV. The migration of
16.
17.
18.
19.
20.
larval Toxocara canis in mice. I. Migration through the intestine in primary infections. Vet Parasitol. 1984;17:65–73. O’Brien DD. Tropical pyomyositis. A manifestation of larva migrans? J R Army Med Corps. 1963;109:43–50. Margareth HD, Smith MD, Beaver PC. Persistence and distribution of toxocara larvae in the tissues of children and mice. Pediatrics. 1953;12:491– 496. Kayes SG, Oaks JA. Development of the granulomatous response in murine toxocariasis. Initial events. Am J Pathol. 1978;93:277–285. McGavin MHD, Krajewska-Pietrasik D, Ryde´n C, Hook M. Identification of a Staphylococcus aureus extracellular matrix-binding protein with broad specificity. Infect Immun. 1993;61:2479 –2485. Del Prete GF, De Carli M, Mastromauro C, et al. Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand in vitro human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production. J Clin Invest. 1991;88:346 –350. Lambertucci JR. Hyperimmunoglobulinemia E, parasitic diseases, and staphylococcal infection. Rev Soc Bras Med Trop. 1996;29:407– 410. Caldwell K, Lobell M, Coccia PF. Mitogenic response to Toxocara antigen and chemotactic defect in visceral larva migrans. Am J Dis Child. 1980;134:845– 847. Ansaloni L, Re MC. High HIV seroprevalence among patients with pyomyositis in Northern Uganda. Trop Med Int Health. 1996;1: 210 –212. Sturchler D, Schubarth P, Gualzata TA, et al. Thiabendazol versus albendazol in treatment of toxocariasis: a clinical trial. Ann Trop Med Parasitol. 1989;83:473– 478. Konate A, Duhamel O, Basset D, et al. Toxocarose et troubles fonctionnels intestinaux. Presentation de 4 cas. Gastroenterol Clin Biol. 1996;20:909 –911.
From the Departments of Internal Medicine (AAR, VN, DMT, JCS, JRL) and Clinical Pathology (GBF), School of Medicine, and the Department of Epidemiology (CMA), Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, Brazil. Correspondence should be addressed to J. R. Lambertucci, MD, PhD, Departamento de Clı´nica Medica, Faculdade de Medicina da UFMG, Av. Alfredo Balena 190, CEP: 30130-100, Belo Horizonte-MG, Brazil. Manuscript submitted January 10, 2000, and accepted in revised form May 31, 2000.
October 1, 2000
THE AMERICAN JOURNAL OF MEDICINE威
Volume 109 425