- Email: [email protected]
Is microsporidial keratitis a seasonal infection in India?
RESEARCH NOTES
Is microsporidial keratitis a seasonal infection in India?
A. K. Reddy1, P. K. Balne1, P. Garg2 and S. Krishnaiah3 1) Jhaveri Microbiology Centre, Hyderabad Eye Research Foundation, 2) Cornea and Anterior Segment Services and 3) International Center for Advancement of Rural Eye Care, L. V. Prasad Eye Institute, Hyderabad, India
Abstract Microsporidia are emerging ocular pathogens. In this study, we describe the seasonal trends of microsporidial keratitis. The incidence of microsporidial keratitis is increasing in India, with a seasonal trend towards disease onset during the monsoon.
Keywords: Incidence, microsporidia, monsoon, seasonal Original Submission: 10 July 2009; Revised Submission: 14 September 2009; Accepted: 5 October 2009 Editor: M. Drancourt Article published online: 14 October 2009 Clin Microbiol Infect 2011; 17: 1114–1116 10.1111/j.1469-0691.2010.03084.x
Corresponding author and reprint requests: A. K. Reddy, Jhaveri Microbiology Centre, Professor Brien A. Holden Eye Research Centre, Hyderabad Eye Research Foundation, L. V. Prasad Eye Institute, Banjara Hills, Hyderabad-500 034, India E-mail: [email protected]
Microsporidia are obligate, intracellular parasites, belonging to the phylum Microspora, and are recognized as opportunistic infectious agents worldwide [1,2]. Human infections caused by microsporidia include intestinal, ocular, sinus, pulmonary, muscular and renal diseases [3]. In 1973, the first case of ocular microsporidiosis was diagnosed in a boy with stromal keratitis [2]. In 1990, several cases of superficial keratitis were seen among AIDS patients; these differed in presentation and clinical course from cases seen earlier in immunocompetent individuals [2]. These individuals had a superficial epithelial keratopathy. In India, the first case of
TROPICAL AND PARASITIC DISEASES
ocular microsporidiosis was reported in 2003, in an immunocompetent individual [4]. Microsporidia are waterborne pathogens [2]. Faecal–oral transmission is the likely route of infection in humans with intestinal microsporidiosis, but the source of ocular infections is not clear [2]. The relatively superficial location of conjunctival and corneal tissues suggests that direct inoculation of the eye may occur [2]. We recently noticed the frequent presentation of new cases of microsporidial keratitis at our institute, prompting us to undertake this study, which aimed to investigate the seasonal trends of microsporidial keratitis. Microbiology records of patients with microsporidial keratitis seen at L. V. Prasad Eye Institute, Hyderabad, India between January 2006 and December 2008 were retrospectively reviewed. The institutional review board of L. V. Prasad Eye Institute has approved this study (Ref. No. LEC08074). Using standard techniques, corneal scrapings were obtained with a sterile no. 15 blade on a Bard Parker handle. Multiple scrapings were collected from each patient for smears and cultures. Scrapings were taken from the lesions, smeared on pre-sterilized slides for staining, and inoculated onto various culture media for growth of bacteria, fungi or Acanthamoeba. The procedure has been described in detail in an earlier publication [5]. The smears were stained with: (i) potassium hydroxide with Calcofluor White (CFW); (ii) Gram stain; (iii) Giemsa stain; and (iv) modified Ziehl– Neelsen stain (Kinyoun’s acid-fast staining). Corneal scrapings from ten patients with microsporidial keratitis were subjected to microsporidial PCR. DNA was extracted from corneal scrapings with the QIAamp DNA kit (Qiagen, Hilden, Germany). Microsporidial PCR was performed using the primers forward C1 (5¢-CACCAGGT TGATTCTGCC-3¢) and reverse C2 (5¢-GTGACGGGC GGTGTGTAC-3¢), which amplifies the four commonly reported species of microsporidia [6]. Amplification was performed in a 25-lL reaction mixture including 2 pmol of each primer, 200 lM each deoxynucleoside triphosphate, 1.5 mM MgCl2, and 1.25 units of Taq DNA polymerase. The PCR programme consisted of: an initial denaturation step at 94C for 3 min; 35 cycles of denaturation at 94C for 45 s, annealing at 57C for 45 s, and extension at 72C for 1 min; and a final extension at 72C for another 7 min. The products of amplification were electrophoretically resolved on a 1.5% agarose gel and visualized for analysis after being stained with ethidium bromide. The expected positive PCR product size was 1200 bp. India has three seasons: monsoon (June to September), winter (October to January) and summer (February to May). The seasonality of microsporidial keratitis was determined by comparing the proportion of cases that pre-
ª2010 The Authors Journal Compilation ª2010 European Society of Clinical Microbiology and Infectious Diseases
Research Notes
CMI
sented in each season, using the chi-square test for proportions. Thirty cases of microsporidial keratitis were identified during the study period. Of these, six were reported in the year 2006, five were reported in the year 2007 and 19 in the year 2008. Of the 30 cases, 20 were reported in the monsoon (June through September), six were reported in winter (October through January) and four were reported in summer (February through May). The proportion of cases reported in each season is shown in Fig. 1. The season of onset of symptoms showed a trend towards the monsoon. The difference between monsoon and summer (66.3% vs. 13.3%; p 0.0004) and the difference between monsoon and winter (66.3% vs. 20.0%; p 0.007) was statistically significant. There was no significant difference between the occurrence in winter and that in summer (20.0% vs. 13.3%; p 0.708). Microsporidial spores were detected by KOH + CFW in 30 of 30 samples (100%), by Gram stain in 20 of 25 (80%), by Giemsa stain in 13 of 17 (76.4%) and by modified Ziehl– Neelsen stain in 26 of 27 (96.2%). Microscopic pictures of microsporidia in KOH + CFW and modified acid-fast (Kinyoun’s acid-fast staining) stain are shown in Fig. 2. Culture was negative for bacteria, fungi and Acanthamoeba in all 30 cases. In ten of 30 patients, corneal scrapings were subjected to microsporidial PCR, and all ten patients were positive for microsporidia in PCR. Ocular infection with microsporidia has been documented both in immunocompetent and in immunosuppressed patients [2,4]. The reported prevalence of microsporidial keratitis was 0.4%, and it is considered to be a rare disease [7]. The incidence of microsporidial keratitis in India is not known, but we noticed an increase in the number of cases of microsporidial keratitis at our tertiary eye-care centre in the last year. This may be due to increased clinical awareness
66.7
70 60 % of cases
50 40 30
20 13.3
20 10 0
Monsoon (June Winter (October Summer through through January) (February September) through May) Season
FIG. 1. Proportion of microsporidial keratitis presenting in each season.
1115
(a)
(b)
FIG. 2. (a) KOH + Calcofluor White stain of corneal scraping showing oval fluorescing microsporidial spores (·40). (b) Modified acid-fast stain (Kinyoun’s method) of corneal scraping, showing oval acid-fast microsporidial spores (·100).
and improved diagnostic capabilities. Recently, Das et al. [8] (Bhubaneswar, India) reported an outbreak of epidemic keratoconjunctivitis with microsporidia. From our study and the study by Das et al., it is clear that there is an increase in the incidence of microsporidial keratitis in India. Variations in the incidence of microsporidial keratitis at different times of the year have not been described previously, except for an outbreak reported by Das et al. Our study points towards an increased incidence of microsporidial keratitis in the monsoon (the months of June, July, August and September). Microsporidia have a worldwide distribution and can be found in any group of animals [9]. Sources and modes of human infection with microsporidia have been difficult to ascertain. Recently, animal reservoirs of microsporidia infecting humans have been confirmed [10,11], but there are no reports of direct transmission of microsporidia from animals to humans. Arthropods are the most common hosts of microsporidia [9]. Human cases of keratitis and myositis caused by Anncaliia algerae (formerly Nosema/Brachiola), a mosquito parasite, have been reported
ª2010 The Authors Journal Compilation ª2010 European Society of Clinical Microbiology and Infectious Diseases, CMI, 17, 1114–1122
1116
Clinical Microbiology and Infection, Volume 17 Number 7, July 2011
[12,13], but there are no reports on ocular infections with other insect-borne microsporidia. The common environmental sources of microsporidia include ditch water and other stagnant water bodies. Three common species of microsporidia that infect humans have been detected in these water samples [1,14]. The increased incidence of microsporidia during the monsoon may be due to contamination of water with microsporidia or the increase in the insect population in this season. The relatively small number of cases and the retrospective nature of the study limit the strength of our conclusions. A prospective study would be required to identify the sources and modes of transmission of microsporidial keratitis and the species of microsporidia responsible for infection.
CMI
13. Visveswara GS, Belloso M, Moura H et al. Isolation of Nosema algerae from the cornea of an immunocompetent patient. J Eukaryot Microbiol 1996; 46: 10S. 14. Sparfel JM, Sarfati C, Liguory O et al. Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR. J Eukaryot Microbiol 1997; 44: 78S.
First entomological documentation of Aedes (Stegomyia) albopictus (Skuse, 1894) in Algeria A. Izri1, I. Bitam2 and R. N. Charrel3 1) Parasitologie-Mycologie, APHP, Hoˆpital Avicenne, Bobigny, France, 2) Entomologie Me´dicale, Institut Pasteur d’Alger, Alger, Alge´rie and 3) Unite´ des Virus Emergents, UMR190, Institut de Recherche pour le
Transparency Declaration
De´veloppement, Universite´ de la Me´diterrane´e, Marseille, France
The study was funded by Hyderabad Eye Research Foundation. The authors declare the absence of competing interests.
Abstract In August 2010, during an entomological programme targeting
References
sandflies, in the region of Larbaa-Nath-Iraten, Wilaya of TiziOuzou (Algeria), a female Aedes albopictus was trapped alive and partially engorged. To our knowledge, this is the first report of
1. Dowd SE, Gerba CP, Pepper IL. Confirmation of human pathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis and Vittaformae cornea in the water. Appl Environ Microbiol 1998; 64: 3332– 3335. 2. Joseph J, Vemuganti GK, Sharma S. Microsporidia: emerging ocular pathogens. Indian J Med Microbiol 2006; 23: 80–91. 3. Weber R, Bryan RT, Schwartz DA, Owen RL. Human microsporidial infections. Clin Microbiol Rev 1994; 7: 426–461. 4. Sridhar MS, Sharma S. Microsporidial keratoconjunctivitis in a HIVseronegative patient treated with debridement and oral itraconazole. Am J Ophthalmol 2003; 136: 745–746. 5. Kunomoto DY, Sharma S, Garg P, Gopinathan U, Miller D, Rao GN. Corneal ulceration in the elderly in Hyderabad, South India. Br J Ophthalmol 2000; 84: 54–59. 6. Raynaud L, Delbac F, Broussolle V et al. Identification of Encephalatozoon intestinalis in travelers with chronic diarrhea by specific PCR amplification. J Clin Microbiol 1998; 36: 37–40. 7. Joseph J, Sridhar MS, Murthy S, Sharma S. Clinical and microbiological profile of microsporidial keratoconjunctivitis in Southern India. Ophthalmology 2006; 113: 531–537. 8. Das S, Sharma S, Sahu SK, Nayak SS, Kar S. New microbial spectrum of epidemic keratoconjunctivitis: clinical and laboratory aspects of outbreak. Br J Ophthalmol 2008; 92: 861–862. 9. Franzen C. Microsporidia: a review of 150 years of research. Open Parasitol J 2008; 2: 1–34. 10. Mathis A, Weber R, Deplazes P. Zoonitic potential of the microsporidia. Clin Microbiol Rev 2005; 18: 423–445. 11. Didier ES, Stovall ME, Green LC, Brindley PJ, Sestak K, Didier PJ. Epidemiology of microsporidiosis: source and modes and transmission. Vet Parasitol 2004; 126: 145–166. 12. Coyle CM, Weiss LM, Rhodes LV et al. Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. N Engl J Med 2004; 351: 42–47.
Ae. albopictus in Algeria and more widely in the Maghreb.
Keywords: Arbovirus, chikungunya, dengue, emergence, virus Original Submission: 12 October 2010; Revised Submission: 2 December 2010; Accepted: 2 December 2010 Editor: G. Greub Article published online: 9 December 2010 Clin Microbiol Infect 2011; 17: 1116–1118 10.1111/j.1469-0691.2010.03443.x
Corresponding author: R. N. Charrel, Unite´ des Virus Emergents, UMR190, Institut de Recherche pour le De´veloppement, Universite´ de la Me´diterrane´e, Faculte´ de Me´decine, 27 blvd Jean Moulin, 13005 Marseille, France E-mail: [email protected]
During an entomological surveillance programme aimed at the collection of sandflies, in the region of Larbaa-Nath-Iraten, Wilaya of Tizi-Ouzou (Algeria), from 2 to 8 August
ª2011 The Authors Clinical Microbiology and Infection ª2011 European Society of Clinical Microbiology and Infectious Diseases, CMI, 17, 1114–1122
Is microsporidial keratitis a seasonal infection in India?
A. K. Reddy1, P. K. Balne1, P. Garg2 and S. Krishnaiah3 1) Jhaveri Microbiology Centre, Hyderabad Eye Research Foundation, 2) Cornea and Anterior Segment Services and 3) International Center for Advancement of Rural Eye Care, L. V. Prasad Eye Institute, Hyderabad, India
Abstract Microsporidia are emerging ocular pathogens. In this study, we describe the seasonal trends of microsporidial keratitis. The incidence of microsporidial keratitis is increasing in India, with a seasonal trend towards disease onset during the monsoon.
Keywords: Incidence, microsporidia, monsoon, seasonal Original Submission: 10 July 2009; Revised Submission: 14 September 2009; Accepted: 5 October 2009 Editor: M. Drancourt Article published online: 14 October 2009 Clin Microbiol Infect 2011; 17: 1114–1116 10.1111/j.1469-0691.2010.03084.x
Corresponding author and reprint requests: A. K. Reddy, Jhaveri Microbiology Centre, Professor Brien A. Holden Eye Research Centre, Hyderabad Eye Research Foundation, L. V. Prasad Eye Institute, Banjara Hills, Hyderabad-500 034, India E-mail: [email protected]
Microsporidia are obligate, intracellular parasites, belonging to the phylum Microspora, and are recognized as opportunistic infectious agents worldwide [1,2]. Human infections caused by microsporidia include intestinal, ocular, sinus, pulmonary, muscular and renal diseases [3]. In 1973, the first case of ocular microsporidiosis was diagnosed in a boy with stromal keratitis [2]. In 1990, several cases of superficial keratitis were seen among AIDS patients; these differed in presentation and clinical course from cases seen earlier in immunocompetent individuals [2]. These individuals had a superficial epithelial keratopathy. In India, the first case of
TROPICAL AND PARASITIC DISEASES
ocular microsporidiosis was reported in 2003, in an immunocompetent individual [4]. Microsporidia are waterborne pathogens [2]. Faecal–oral transmission is the likely route of infection in humans with intestinal microsporidiosis, but the source of ocular infections is not clear [2]. The relatively superficial location of conjunctival and corneal tissues suggests that direct inoculation of the eye may occur [2]. We recently noticed the frequent presentation of new cases of microsporidial keratitis at our institute, prompting us to undertake this study, which aimed to investigate the seasonal trends of microsporidial keratitis. Microbiology records of patients with microsporidial keratitis seen at L. V. Prasad Eye Institute, Hyderabad, India between January 2006 and December 2008 were retrospectively reviewed. The institutional review board of L. V. Prasad Eye Institute has approved this study (Ref. No. LEC08074). Using standard techniques, corneal scrapings were obtained with a sterile no. 15 blade on a Bard Parker handle. Multiple scrapings were collected from each patient for smears and cultures. Scrapings were taken from the lesions, smeared on pre-sterilized slides for staining, and inoculated onto various culture media for growth of bacteria, fungi or Acanthamoeba. The procedure has been described in detail in an earlier publication [5]. The smears were stained with: (i) potassium hydroxide with Calcofluor White (CFW); (ii) Gram stain; (iii) Giemsa stain; and (iv) modified Ziehl– Neelsen stain (Kinyoun’s acid-fast staining). Corneal scrapings from ten patients with microsporidial keratitis were subjected to microsporidial PCR. DNA was extracted from corneal scrapings with the QIAamp DNA kit (Qiagen, Hilden, Germany). Microsporidial PCR was performed using the primers forward C1 (5¢-CACCAGGT TGATTCTGCC-3¢) and reverse C2 (5¢-GTGACGGGC GGTGTGTAC-3¢), which amplifies the four commonly reported species of microsporidia [6]. Amplification was performed in a 25-lL reaction mixture including 2 pmol of each primer, 200 lM each deoxynucleoside triphosphate, 1.5 mM MgCl2, and 1.25 units of Taq DNA polymerase. The PCR programme consisted of: an initial denaturation step at 94C for 3 min; 35 cycles of denaturation at 94C for 45 s, annealing at 57C for 45 s, and extension at 72C for 1 min; and a final extension at 72C for another 7 min. The products of amplification were electrophoretically resolved on a 1.5% agarose gel and visualized for analysis after being stained with ethidium bromide. The expected positive PCR product size was 1200 bp. India has three seasons: monsoon (June to September), winter (October to January) and summer (February to May). The seasonality of microsporidial keratitis was determined by comparing the proportion of cases that pre-
ª2010 The Authors Journal Compilation ª2010 European Society of Clinical Microbiology and Infectious Diseases
Research Notes
CMI
sented in each season, using the chi-square test for proportions. Thirty cases of microsporidial keratitis were identified during the study period. Of these, six were reported in the year 2006, five were reported in the year 2007 and 19 in the year 2008. Of the 30 cases, 20 were reported in the monsoon (June through September), six were reported in winter (October through January) and four were reported in summer (February through May). The proportion of cases reported in each season is shown in Fig. 1. The season of onset of symptoms showed a trend towards the monsoon. The difference between monsoon and summer (66.3% vs. 13.3%; p 0.0004) and the difference between monsoon and winter (66.3% vs. 20.0%; p 0.007) was statistically significant. There was no significant difference between the occurrence in winter and that in summer (20.0% vs. 13.3%; p 0.708). Microsporidial spores were detected by KOH + CFW in 30 of 30 samples (100%), by Gram stain in 20 of 25 (80%), by Giemsa stain in 13 of 17 (76.4%) and by modified Ziehl– Neelsen stain in 26 of 27 (96.2%). Microscopic pictures of microsporidia in KOH + CFW and modified acid-fast (Kinyoun’s acid-fast staining) stain are shown in Fig. 2. Culture was negative for bacteria, fungi and Acanthamoeba in all 30 cases. In ten of 30 patients, corneal scrapings were subjected to microsporidial PCR, and all ten patients were positive for microsporidia in PCR. Ocular infection with microsporidia has been documented both in immunocompetent and in immunosuppressed patients [2,4]. The reported prevalence of microsporidial keratitis was 0.4%, and it is considered to be a rare disease [7]. The incidence of microsporidial keratitis in India is not known, but we noticed an increase in the number of cases of microsporidial keratitis at our tertiary eye-care centre in the last year. This may be due to increased clinical awareness
66.7
70 60 % of cases
50 40 30
20 13.3
20 10 0
Monsoon (June Winter (October Summer through through January) (February September) through May) Season
FIG. 1. Proportion of microsporidial keratitis presenting in each season.
1115
(a)
(b)
FIG. 2. (a) KOH + Calcofluor White stain of corneal scraping showing oval fluorescing microsporidial spores (·40). (b) Modified acid-fast stain (Kinyoun’s method) of corneal scraping, showing oval acid-fast microsporidial spores (·100).
and improved diagnostic capabilities. Recently, Das et al. [8] (Bhubaneswar, India) reported an outbreak of epidemic keratoconjunctivitis with microsporidia. From our study and the study by Das et al., it is clear that there is an increase in the incidence of microsporidial keratitis in India. Variations in the incidence of microsporidial keratitis at different times of the year have not been described previously, except for an outbreak reported by Das et al. Our study points towards an increased incidence of microsporidial keratitis in the monsoon (the months of June, July, August and September). Microsporidia have a worldwide distribution and can be found in any group of animals [9]. Sources and modes of human infection with microsporidia have been difficult to ascertain. Recently, animal reservoirs of microsporidia infecting humans have been confirmed [10,11], but there are no reports of direct transmission of microsporidia from animals to humans. Arthropods are the most common hosts of microsporidia [9]. Human cases of keratitis and myositis caused by Anncaliia algerae (formerly Nosema/Brachiola), a mosquito parasite, have been reported
ª2010 The Authors Journal Compilation ª2010 European Society of Clinical Microbiology and Infectious Diseases, CMI, 17, 1114–1122
1116
Clinical Microbiology and Infection, Volume 17 Number 7, July 2011
[12,13], but there are no reports on ocular infections with other insect-borne microsporidia. The common environmental sources of microsporidia include ditch water and other stagnant water bodies. Three common species of microsporidia that infect humans have been detected in these water samples [1,14]. The increased incidence of microsporidia during the monsoon may be due to contamination of water with microsporidia or the increase in the insect population in this season. The relatively small number of cases and the retrospective nature of the study limit the strength of our conclusions. A prospective study would be required to identify the sources and modes of transmission of microsporidial keratitis and the species of microsporidia responsible for infection.
CMI
13. Visveswara GS, Belloso M, Moura H et al. Isolation of Nosema algerae from the cornea of an immunocompetent patient. J Eukaryot Microbiol 1996; 46: 10S. 14. Sparfel JM, Sarfati C, Liguory O et al. Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR. J Eukaryot Microbiol 1997; 44: 78S.
First entomological documentation of Aedes (Stegomyia) albopictus (Skuse, 1894) in Algeria A. Izri1, I. Bitam2 and R. N. Charrel3 1) Parasitologie-Mycologie, APHP, Hoˆpital Avicenne, Bobigny, France, 2) Entomologie Me´dicale, Institut Pasteur d’Alger, Alger, Alge´rie and 3) Unite´ des Virus Emergents, UMR190, Institut de Recherche pour le
Transparency Declaration
De´veloppement, Universite´ de la Me´diterrane´e, Marseille, France
The study was funded by Hyderabad Eye Research Foundation. The authors declare the absence of competing interests.
Abstract In August 2010, during an entomological programme targeting
References
sandflies, in the region of Larbaa-Nath-Iraten, Wilaya of TiziOuzou (Algeria), a female Aedes albopictus was trapped alive and partially engorged. To our knowledge, this is the first report of
1. Dowd SE, Gerba CP, Pepper IL. Confirmation of human pathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis and Vittaformae cornea in the water. Appl Environ Microbiol 1998; 64: 3332– 3335. 2. Joseph J, Vemuganti GK, Sharma S. Microsporidia: emerging ocular pathogens. Indian J Med Microbiol 2006; 23: 80–91. 3. Weber R, Bryan RT, Schwartz DA, Owen RL. Human microsporidial infections. Clin Microbiol Rev 1994; 7: 426–461. 4. Sridhar MS, Sharma S. Microsporidial keratoconjunctivitis in a HIVseronegative patient treated with debridement and oral itraconazole. Am J Ophthalmol 2003; 136: 745–746. 5. Kunomoto DY, Sharma S, Garg P, Gopinathan U, Miller D, Rao GN. Corneal ulceration in the elderly in Hyderabad, South India. Br J Ophthalmol 2000; 84: 54–59. 6. Raynaud L, Delbac F, Broussolle V et al. Identification of Encephalatozoon intestinalis in travelers with chronic diarrhea by specific PCR amplification. J Clin Microbiol 1998; 36: 37–40. 7. Joseph J, Sridhar MS, Murthy S, Sharma S. Clinical and microbiological profile of microsporidial keratoconjunctivitis in Southern India. Ophthalmology 2006; 113: 531–537. 8. Das S, Sharma S, Sahu SK, Nayak SS, Kar S. New microbial spectrum of epidemic keratoconjunctivitis: clinical and laboratory aspects of outbreak. Br J Ophthalmol 2008; 92: 861–862. 9. Franzen C. Microsporidia: a review of 150 years of research. Open Parasitol J 2008; 2: 1–34. 10. Mathis A, Weber R, Deplazes P. Zoonitic potential of the microsporidia. Clin Microbiol Rev 2005; 18: 423–445. 11. Didier ES, Stovall ME, Green LC, Brindley PJ, Sestak K, Didier PJ. Epidemiology of microsporidiosis: source and modes and transmission. Vet Parasitol 2004; 126: 145–166. 12. Coyle CM, Weiss LM, Rhodes LV et al. Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. N Engl J Med 2004; 351: 42–47.
Ae. albopictus in Algeria and more widely in the Maghreb.
Keywords: Arbovirus, chikungunya, dengue, emergence, virus Original Submission: 12 October 2010; Revised Submission: 2 December 2010; Accepted: 2 December 2010 Editor: G. Greub Article published online: 9 December 2010 Clin Microbiol Infect 2011; 17: 1116–1118 10.1111/j.1469-0691.2010.03443.x
Corresponding author: R. N. Charrel, Unite´ des Virus Emergents, UMR190, Institut de Recherche pour le De´veloppement, Universite´ de la Me´diterrane´e, Faculte´ de Me´decine, 27 blvd Jean Moulin, 13005 Marseille, France E-mail: [email protected]
During an entomological surveillance programme aimed at the collection of sandflies, in the region of Larbaa-Nath-Iraten, Wilaya of Tizi-Ouzou (Algeria), from 2 to 8 August
ª2011 The Authors Clinical Microbiology and Infection ª2011 European Society of Clinical Microbiology and Infectious Diseases, CMI, 17, 1114–1122