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Serotypes of Vibrio cholerae Non-O1 Isolated from Water Supplies for Human Consumption in Campeche, México and their Antibiotic Susceptibility Pattern

Abstract

The presence of Vibrio cholerae non-O1 in water supplies for human consumption in the city of Campeche and rural locality of Bécal was investigated. V. cholerae non-O1 was detected in 5.9% of the samples obtained in deep pools of Campeche. Studies conducted in Bécal and neighbourhood of Morelos in Campeche indicated that collected samples harbored V. cholerae non-O1 in 31.5% and 8.7% respectively. There was a particular pattern of distribution of V. cholerae non-O1 serotypes among different studied regions. Accordingly, V. cholerae non-O1 serotype O14 predominated in the deep pools of Campeche and together with V. cholerae non-O1, O155 were preferentially founds in samples taken from intradomiciliary faucets in the neighbourhood of Morelos. Samples from Bécal predominantly presented the serotype O112. 60% and 53.8% of all studied strains of V. cholerae non-O1 proved to be resistant to ampicillin and carbenicillin. 3.1%, 7.7% and 6.2% presented resistant to doxycycline, trimethoprim-sulfamethoxazole and erythromycin respectively. The study showed the necessity of performing a strong epidemiologic surveillance for emergence and distribution of V. cholerae non-O1

Vibrio cholerae non-O1; serotypes; antibiotic susceptibility; water supplies; Campeche; México


Serotypes of Vibrio cholerae Non-O1 Isolated from Water Supplies for Human Consumption in Campeche, México and their Antibiotic Susceptibility Pattern

Vol. 93(1): 17-22

Angélica P Isaac-Márquez/+, Claudio M Lezama-Dávila*, Carlos Eslava-

Campos**, Armando Navarro-Ocaña**, Alejandro Cravioto-Quintana**

Centro de Investigaciones en Enfermedades Tropicales, Universidad Autónoma de Campeche, Av. Agustín Melgar s/n, 24030, Campeche, México *Laboratorio de Patología Experimental, Facultad de Medicina, Universidad Autónoma de Yucatán, Av. Itzaes 498, 97000, Mérida, Yucatán, México **Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510, México, D.F.

The presence of Vibrio cholerae non-O1 in water supplies for human consumption in thecity of Campeche and rural localityof Bécal was investigated. V. cholerae non-O1 was detected in 5.9% of the samples obtained in deep pools of Campeche. Studies conducted in Bécal and neighbourhood of Morelos in Campeche indicated that collected samples harbored V. cholerae non-O1 in 31.5% and 8.7% respectively. There was a particular pattern of distribution of V. cholerae non-O1 serotypes among different studied regions. Accordingly, V. cholerae non-O1 serotype O14 predominated in the deep pools of Campeche and together with V. cholerae non-O1, O155 were preferentially founds in samples taken from intradomiciliary faucets in the neighbourhood of Morelos. Samples from Bécal predominantly presented the serotype O112. 60% and 53.8% of all studied strains of V. cholerae non-O1 proved to be resistant to ampicillin and carbenicillin. 3.1%, 7.7% and 6.2% presented resistant to doxycycline, trimethoprim-sulfamethoxazole and erythromycin respectively. The study showed the necessity of performing a strong epidemiologic surveillance for emergence and distribution of V. cholerae non-O1.

Key words: Vibrio cholerae non-O1 - serotypes - antibiotic susceptibility - water supplies - Campeche - México

Vibrio cholerae serogroup non-O1 are autochthonous bacteria of aquatic environments (Morris 1990) and right from the 1950s and 1960s has been identified in outbreaks of gastroenteritis in different parts of the world (McIntyre et al. 1965, Aldová et al. 1968, El-Shawi & Thewaini 1969, Kamal 1971). Currently it is recognized that non-O1 serogroup includes approximately 150 serotypes and play an important role as an aethiological agent of gastrointestinal illness ranging from mild watery diarrhea to febrile enteritis with bloody diarrhea. In contrast to V. cholerae O1, V. cholerae non-O1 causes extraintestinal infections (Sanyal 1992); but gastroenteritis is the most common clinical manifestation (Morris 1990, WHO 1993).

In October 1992, an epidemic of cholera-like illness caused by a V. cholerae serogroup non-O1 broke in Madras, India. The causative agent was found to be a new serogroup of V. cholerae, defined as O139, with the synonym Bengal, in recognition of the origin of this strain (Shimada et al. 1993, Ramamurthy et al. 1993). This strain has also been responsible for epidemic outbreaks of cholera in Bangladesh, southern Asia and U.S.A. (Albert et al. 1993, Bhattacharya et al. 1993, CDC 1993, Gonzalez et al. 1993) with possible disemination to Latin America throughout imported cases.Before of this epidemics of V. cholerae non-O1, O139 only V. cholerae O1 was considered capable of producing epidemics of cholera.

In Peru, cholera appeared in January 1991 and spreaded quickly in Latin America (PAHO 1995). The disease evolved in explosive epidemics, the largest recorded since the beginning of the seventh pandemic in Indonesia in 1961. The first reported cases of cholera in the state of Campeche, located in southeast of México, were registered in August 1991 and because of a number of environmental conditions determined by economic, sociologic and educational factors, this disease spread quickly and from 1992 became one of the federal states with more reported cases of this disease, registering the first places in morbility and mortality rates in México (DGE 1993, 1995, Valdespino 1994).

From 1992 up to now city of Campeche has experienced several outbreaks of cholera and from July to September, 1993 Bécal, rural locality of Campeche, registered an important number of cases of this disease. The purpose of this study was the characterization of serotypes and the antibiotic susceptibility pattern of V. cholerae non-O1 strains isolated from water supplies for human consumption before, during and after those outbreaks of cholera.

This study was performed in three different steps. The first one was from August 1992 to July 1993 and included seven samplings of water coming from 35 deep pools that provide water to the city of Campeche. The second step was carried out during August to December 1993 and included two collections of samples from the distribution network placed in the rural locality of Bécal. In addition, were examined intradomiciliary deep pools and rainwater cistern systems which are commonly used in this region for human consumption. The third step was performed during July 1994 to February 1995 and included two water monitorings of neighbourhood of Morelos in the city of Campeche.

Testing of total residual chlorine concentra-

tion - Presence of total residual chlorine in water samples was evaluated by the ortotoluidine method (Rodier 1990). Chlorine concentration studied varied from 0 to 3 ppm.

Isolation - The Spira swab (Spira & Ahmed 1981) and double enrichment in alkaline peptone water (Chandra 1992) methods were used for the isolation of V. cholerae. In both cases were employed the TCBS agar (thiosulfate-citrate-bile-sucrose agar). The water samples were storaged and transported at 4oC and processed within the next 2 hr of their collection.

Identification - Yellow colonies from TCBS agar were submitted to the standard series of biochemical media used for identification of members of the Vibrionaceae family (Holt et al. 1994). The serological identification was determined by slide agglutination test using polyvalent O1 and type-specific Inaba and Ogawa antisera (Difco) and by coagglutination test employing monoclonal antibody anti-V.cholerae O1 adsorbed to heat-killed S. aureus (New Horizons Diagnostics Co.). V. cholerae serogroup O1 and non-O1 were used as controls.

Serological classification of V. cholerae non-O1 - Polyvalent antisera for serological classification of different V. cholerae non-O1 serotypes were used. The reference strains of V. cholerae non-O1 serotypes O1 to O83 were kindly provided by Dr Bernard Rowe, Head of Enteric Pathogens Central Laboratory of Public Health, London, England, and those reference strains from serotype O84 to O140 and O155 were provided by Dr T Shimada from the National Institute of Health, Tokyo, Japan. Antigens used for serological classification were obtained by heating bacterial cultures at 100oC for 1 hr and adjusted with tube 3 of McFarland nephelometer; 1:100 serum dilutions were used in a proportion of antigen/sera (V/V) of 50 ml in 96 wells microtitration plates, incubated at 50oC for 24 hr. Sera that agglutinated with this antigen preparation was serially diluted twice to know the titer and so determinate identity of each serotype (Sakazaki & Donovan 1984, Shimada et al. 1994).

Antimicrobial susceptibility testing - All V. cholerae non-O1 isolates were tested for antibiotic susceptibility to 15 antibiotics (Difco) by Kirby-Bauer method (NCCLS 1988) and strains were recorded as susceptible, intermediate, moderately susceptible or resistant.

The results indicate that in 41.1% (14/34) and 80.7% (67/83) of the samples collected from intradomiciliary faucets of rural locality of Bécal and neighbourhood of Morelos a range of 0.5- 1.5 ppm and 0.3-3 ppm of total residual chlorine was detected, respectively, by the ortotoluidine method. In the case of deep pools in Morelos and Bécal, 76.9% (10/13) and 12.5% (1/8) of samples collected presented a range of 1-3 ppm. Samples obtained both from deep pools in Campeche and from the distribution tanks, intradomiciliary deep pools and rainwater cistern systems in the studied areas did not contained chlorine.

In Table I it is shown the frequency of isolation of V. cholerae non-O1 strains in different water sources. 5.9% (13/222) of water samples taken from deep pools of the city of Campeche, and 31.5% (17/54) and 8.7% (9/104) of those water samples from Bécal and Morelos respectively harbored V. cholerae non-O1.

Biochemical features of isolated strains were very similar to those reported by Holt et al. (1994). It has been reported that V. cholerae do not perform esculin hydrolysis, however, 67.7% (44/65) of those strains isolated can indeed to hydrolize this compound at 0 and 1% of sodium chloride. In addition, 3.1% (2/65) of bacterial strains grew in nutrient agar with 8% of NaCl.

A total of 65 strains belonging to 29 different serotypes were identified during the period of study. In Table II it is shown the distribution and frequency of V. cholerae non-O1 serotypes in relation to the total of bacterial strains isolated in the studied regions. The 35.7% (5/14) of samples analyzed from deep pools in Campeche contained V. cholerae non-O1 serotype O14. In the neighbourhood of Morelos 33.3% (3/9) and 22.2% (2/9) of samples taken from intradomiciliary faucets harbored V. cholerae serotypes O155 and O14 respectively.

Only in one out of three deep pools of Bécal was isolated V. cholerae non-O1 serotype O112 in all the tested samples. Additionaly, in 66.7% (2/3) of those samples were isolated bacterias that biochemically behave as V. cholerae non-O1 but did not agglutinate with any of the 141 anti-V. cholerae non-O1 polyvalent sera (anti-V. cholerae non-O1 serotype O1 to O140 and O155) availables. In 80% (8/10) of tested samples of intradomiciliary faucets was detected V. cholerae non-O1 serotype O112.

The water samples taken from the intradomi-ciliary deep pools in Bécal registered the presence of V. cholerae non-O1 serotypes O58, O38, O8 and O4. It was demonstrated the presence of V. cholerae non-O1 serotype O98 in rainwater cistern systems.

The pattern of susceptibility of 65 isolated strains of V. cholerae non-O1 with 15 different antibiotics is shown in Table III. More than 67.7% (44/65) of the isolated strains were susceptible to the aminoglycosides, cephalosporins, tetracyclines, chloramphenicol, nitrofurantoin and trimethoprim-sulfamethoxazole. In contrast, 50.8% (33/65) of all strains showed resistance to two or more drugs. 49.2% (32/65) of these microorganisms were resistant to ampicillin and carbenicillin, while 10.8% (7/65) were resistant only to ampicillin and 4.6% (3/65) exhibited resistance only to carbenicillin. The rate of resistance to these substances was higher than to the other drugs. In addition, 3.1% (2/65), 7.7% (5/65) and 6.2% (4/65) of V. cholerae non-O1 strains presented resistance to the doxycycline, trimethoprim-sulfamethoxazole and erythromycin respectively.

Based in the results of the present study it is possible to conclude that the water distribution system plays an important role as transmission vehicle for V. cholerae non-O1. Considering the presence of V. cholerae non-O1 in the studied sources, it is possible to assume that this organism might be responsible of a proportion of diarrheal diseases among the population of the city of Campeche and the rural locality of Bécal.

It is important to observe that 29 V. cholerae non-O1 serotypes found in this study display a clear pattern of geographic distribution. As can be observed in the Table II V. cholerae non-O1, O112 was located only in Bécal, and V. cholerae non-O1, O14 and O155 were exclusively located in the city of Campeche. Regarding to those serotypes with a less frequent presentation; those present in Bécal are different to the ones found in the city of Campeche with only one exception that corresponded to V. cholerae non-O1, O7. V. cholerae non-O1, O14 and O35 were present in samples taken from city of Campeche and neighbourhood of Morelos, nonetheless the serotypes of the remaining strains were different.

Additionaly, 9.1% (3/33) and 4.8% (1/21) of those strains isolated in Bécal and the city of Campeche, respectively belong to a particular V. cholerae non-O1 strain which do not corresponded to any of those 141 serotypes that were studied in this work and might represent an autoctonous uncharacterized serotypes.

The presence of 2 or 3 different serotypes of V. cholerae non-O1 were detected in 21.4% (3/14), 22.0% (2/9) and 29.4% (5/17) of samples collected from the city of Campeche, neighbourhood of Morelos and the rural locality of Bécal respectively. This indicate that coexistance of different serotypes of V. cholerae non-O1 frequently happens within the same habitat.

Nonetheless that a high percentage of strains isolated during the development of this study displayed susceptibility to a diverse group of antibiotics, it is important to observe that V. cholerae non-O1 strains presented an important resistance to doxycycline, trimethoprim-sulfamethoxazole and erithromycin. Additionaly, a hight percentage of those strains registered an intermediate susceptibility to erithromycin and tetracycline. This susceptibility pattern represent a significant information because they are the antibiotics that WHO recommends for the treatment of cholera. In México during 1991, 3.2% of clinical isolates of V. cholerae O1 presented resistance to tetracycline and 1.5% to doxycycline. During 1992 this multiresistance decreased to 1.4% and from 1993 to 1995 only 0.1% of V. cholerae O1 strains registered resistance to the antibiotics mentioned; nonetheless the strains isolated conserved their resistance to ampicillin (Gutiérrez-Cogio 1995). In México, there is not available information about antibiotic susceptibility pattern of environmental isolates of V. cholerae non-O1. However, according to the results obtained in this study it is possible to conclude that the environmental V. cholerae non-O1 strains are significantly more resistant to antibiotics than the clinical V. cholerae O1 strains. This acquired an important significance, because of phenomenon of acquired plasmid-mediated resistance that might occur in a habitat where V. cholerae serogroup O1 and non-O1 coexists. Studies performed in Tanzania and Bangladesh reported strains of V. cholerae with plasmid-mediated resistance to a wide range of antibiotics (Mhalu et al. 1979, Threlfall & Rowe 1982).

Dalsgaard et al. (1995) reported that of 23 environmental V. cholerae non-O1 strains, 78.3% exhibited resistance to tetracycline and 8.7% were resistant to ampicillin and chloramphenicol. These results differ from the results of the present study. Nevertheless, the resistance to trimethoprim/sulfamethoxazole and erythromycin were similar in both studies. It is possible that variations in the antibiotic susceptibility pattern could be connected with the origin and habitat conditions of the V. cholerae non-O1 strains and with a variety of antibiotics used in differents parts of the world.

The sudden emergence of V. cholerae non-O1, O139 as ethiologic agent of epidemic cholera represents an important shift in the epidemiology of this disease. The evidence suggests the V. cholerae O1 El Tor gave rise to O139 by adquisition of novel DNA (Colwell 1996). Studies have shown that DNA sequence that determine the antigenic properties of the O139 cell surface is also present in two V. cholerae non-O1 strains with serotypes O69 and O141 (Colwell 1996) and additionaly that V. cholerae non-O1 serotypes O22 and O155 posses somatic (O) antigen factors in common with O139 strain (Mukhopadhyay et al. 1995). Cravioto et al. (1994) proved that the Bengal strain is genetically related to V. cholerae O1 El Tor Ogawa isolated in México, and two other non-O1 strains (serotypes O22 and O30). In the present study V. cholerae serotypes O30 and O155 were detected in samples analyzed in the city of Campeche. Considering these finding, it is not possible to establish a line of division between V. cholerae O1, O139 and the bacterial strains belonging to serogroup non-O1. It is now evident that these microorganisms have acquired an increasing importance, particularly in relation to medical relevance and ecological distribution.

The fact that the serogroup O139 emerged as responsible of epidemic cholera raised the possibility that such an event can occur once again, in relation to V. cholerae non-O1 serotypes prevalents in the Americas. It is recommended a strong epidemiologic surveillance in particular regarding emergence and distribution of V. cholerae non-O1 strains both in environmental samples and clinical specimens. Additional support to these study is found in the fact that V. cholerae non-O1 has been isolated in patients with diarrhoea in México (Gutiérrez-Cogio 1995). In addition, the relatively high prevalence of multiple antibiotic resistance of V. cholerae non-O1 strains recovered from water samples indicate the necessity of performing a epidemiologic surveillance of the pattern of antibiotic susceptibility.

To health authorities and the government of Campeche for the assistance provided during the development of this study. To the staff of the University of Campeche for technical assistance.

  • Albert MJ, Siddique AK, Islam MS, Faruque AS, Ansaruzzaman M, Faruque SM, Sack RB 1993. Large outbreak of clinical cholera due to

    Vibrio cholerae non-O1 in Bangladesh [letter].

    Lancet 341: 704.

  • Aldová E, Laznickova K, Stepankova E, Lietava J 1968. Isolation of nonagglutinable vibrios from an enteritis outbreak in Czechoslovakia.

    J Infect Dis 118: 25-31.

  • Bhattacharya MK, Bhattacharya SK, Garg S, Saha PK, Dutta D, Nair GB, Deb BC, Das KP 1993. Outbreak of

    Vibrio cholerae non-O1 in India and Bangladesh [letter].

    Lancet 341: 1346-1347.

  • CDC-Centers for Disease Control 1993. Imported cholera associated with a newly described toxigenic

    Vibrio cholerae O139 strain-California, 1993.

    Morbid Mortal Weekly Rep 42: 501-503.

  • Chandra Pal S 1992. Laboratory diagnosis, p. 229-251. In D Barua, WB III Greenough (eds),

    Cholera, Plenum Medical Book Company, New York.

  • Colwell RR 1996. Global climate and infectious disease: the cholera paradigm.

    Science

    274: 2025-2031.

  • Cravioto A, Beltrán P, Delgado G, Navarro A, Eslava C, León S, González AR 1994. Non-O1

    Vibrio cholerae O139 Bengal is genetically related to

    V. cholerae O1 El Tor Ogawa isolated in Mexico.

    J Infect Dis 169: 1412-1413.

  • Dalsgaard A, Serichantalergs O, Pitarangsi C, Echeverria P 1995. Molecular characterization and antibiotic susceptibility of

    Vibrio cholerae non-O1.

    Epidemiol Infect 114: 51-63.

  • DGE-Dirección General de Epidemiología 1993. Situación del cólera en México. Diciembre de 1992 (editorial).

    Boletín Mensual de Epidemiología 8: 10-13.

  • DGE-Dirección General de Epidemiología 1995. Casos nuevos por entidad federativa de enfermedades diarreicas agudas hasta la semana 50; cólera y SIDA hasta la semana 52 de 1995 (editorial).

    Epi-demiología 12: 7.

  • El-Shawi N, Thewaini AJ 1969. Non-agglutinable vibrios isolated in the 1966 epidemic of cholera in Iraq.

    Bull WHO 40: 163-166.

  • Gonzalez BC, Villanueva Z, Gutierrez CL, Figueroa P, Giono CS, Velazquez VL 1993. Cambios en la epidemiología mundial del cólera. Difusión de

    Vibrio cholerae no O1, O139.

    Bol Cólera/Diarreas Infecciosas 3: 419.

  • Gutiérrez-Cogio L 1995. Variación de las cepas de

    Vibrio cholerae aisladas en la República Mexicana entre 1991 y 1995.

    Epidemiología 12: 1-2.

  • Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST 1994.

    Bergey's manual of determinative bacteriology, p. 273-274. 9th ed., Williams & Wilkins, Baltimore, U.S.A.

  • Kamal AM 1971. Outbreak of gastroenteritis by nonagglutinable (NAG) vibrios in the Republic of Sudan.

    J Egypt Public Health Assoc 46: 125-173.

  • McIntyre OR, Feeley JC, Greenough WB III, Benenson AS, Hassan SI, Saad A 1965. Diarrhea caused by non-cholera vibrios.

    Am J Trop Med Hyg 14: 412-418.

  • Mhalu FS, Mmari PW, Ijumba J 1979. Rapid emergence of El Tor

    Vibrio cholerae resistant to antimicrobial agents during first six months of fourth cholera epidemic in Tanzania.

    Lancet i: 345-347.

  • Morris JG Jr 1990. Non-O group 1

    Vibrio cholerae: a look at the epidemiology of an occasional pathogen.

    Epidemiol Rev 12: 179-191.

  • Mukhopadhyay AK, Saha PK, Garg S, Bhattacharya SK, Shimada T, Takeda T, Takeda Y, Nair GB 1995. Distribution and virulence of

    Vibrio cholerae belonging to serogroups other than O1 and O139: a nation wide survey.

    Epidemiol Infect 114: 65-70.

  • NCCLS-National Committee for Clinical Laboratory Standards 1988. Performance standards for antimicrobial disk susceptibility tests k, de. 4, M2-T4; 8: 75-87.

  • PAHO-Pan-American Health Organization 1995. Cholera in the Americas.

    Epidemiol Bull 16: 11-13.

  • Ramamurthy T, Garg S, Sharma R, Bhattacharya SK, Nair GB, Shimada T, Takeda T, Karasawa T, Kurazano H, Pal A, Takeda Y 1993. Emergence of novel strain of

    Vibrio cholerae with epidemic potential in southern and eastern India [letter].

    Lancet 341: 703-704.

  • Rodier J 1990.

    Análisis de las aguas. Aguas naturales, aguas residuales y agua de mar, p. 476-478, 2da. reimpresión, Ediciones Omega, S.A., Barcelona, España.

  • Sakazaki R, Donovan JT 1984. Serology and epidemiology of

    V. cholerae and

    V. mimicus.

    Meth Microbiol 16: 271-289.

  • Sanyal SC 1992. Epidemiology and pathogenicity of non-O1

    Vibrio species and related organisms, p. 57-67. In D Barua, WB III Greenough (eds),

    Cholera, Plenum Medical Book Company, New York.

  • Shimada T, Arakawa E, Itoh K, Okitsu T, Matsushima A, Asai Y, Yamai S, Nakazato T, Nair GB, Albert MJ, Takeda Y 1994. Extended serotyping scheme for

    V. cholerae.

    Curr Microbiol 28: 175-178.

  • Shimada T, Nair GB, Deb BC, Albert MJ, Sack RB, Takeda Y 1993. Outbreaks of

    Vibrio cholerae non-O1 in India and Bangladesh [letter].

    Lancet 341: 1347.

  • Spira WM, Ahmed QS 1981. Gauze filtration and enrichment procedures for recovery of

    Vibrio cholerae from contaminated waters.

    Appl Environ Microbiol 42: 730-733.

  • Threlfall EJ, Rowe B 1982.

    Vibrio cholerae El Tor acquires plasmied-encoded resistance to gentamicin.

    Lancet i: 42.

  • Valdespino Gómez JL 1994. Cólera, p.169-178. In JL Valdespino Gómez, O Velasco Castrejón, A Escobar Gutierrez, A Del Río Zolezzi, S Ibañez Bernal, C Magos López (eds)

    Enfermedades Tropicales en México. Diagnóstico, tratamiento y distribución geográfica. Instituto Nacional de Diagnóstico y Referencia Epidemiológicos, México, D.F.

  • WHO 1993. Epidemic diarrhea due to

    Vibrio cholerae non-O1.

    Wkly Epidemiol Rec 68: 141-142.

This work was finantially supported by Secretaría de Educación Pública (C 91-01-04-002-441, P/FOMES 93-04-01 and P/FOMES 94-04-03-01), the National University of México and the University of Campeche.

+Corresponding author. Fax: +52-981-1-42-76

Received 5 March 1997

Accepted 27 August 1997

  • Albert MJ, Siddique AK, Islam MS, Faruque AS, Ansaruzzaman M, Faruque SM, Sack RB 1993. Large outbreak of clinical cholera due to Vibrio cholerae non-O1 in Bangladesh [letter]. Lancet 341: 704.
  • Aldová E, Laznickova K, Stepankova E, Lietava J 1968. Isolation of nonagglutinable vibrios from an enteritis outbreak in Czechoslovakia. J Infect Dis 118: 25-31.
  • Bhattacharya MK, Bhattacharya SK, Garg S, Saha PK, Dutta D, Nair GB, Deb BC, Das KP 1993. Outbreak of Vibrio cholerae non-O1 in India and Bangladesh [letter]. Lancet 341: 1346-1347.
  • CDC-Centers for Disease Control 1993. Imported cholera associated with a newly described toxigenic Vibrio cholerae O139 strain-California, 1993. Morbid Mortal Weekly Rep 42: 501-503.
  • Chandra Pal S 1992. Laboratory diagnosis, p. 229-251. In D Barua, WB III Greenough (eds), Cholera, Plenum Medical Book Company, New York.
  • Colwell RR 1996. Global climate and infectious disease: the cholera paradigm. Science 274: 2025-2031.
  • Cravioto A, Beltrán P, Delgado G, Navarro A, Eslava C, León S, González AR 1994. Non-O1 Vibrio cholerae O139 Bengal is genetically related to V. cholerae O1 El Tor Ogawa isolated in Mexico. J Infect Dis 169: 1412-1413.
  • Dalsgaard A, Serichantalergs O, Pitarangsi C, Echeverria P 1995. Molecular characterization and antibiotic susceptibility of Vibrio cholerae non-O1. Epidemiol Infect 114: 51-63.
  • DGE-Dirección General de Epidemiología 1993. Situación del cólera en México. Diciembre de 1992 (editorial). Boletín Mensual de Epidemiología 8: 10-13.
  • DGE-Dirección General de Epidemiología 1995. Casos nuevos por entidad federativa de enfermedades diarreicas agudas hasta la semana 50; cólera y SIDA hasta la semana 52 de 1995 (editorial). Epi-demiología 12: 7.
  • El-Shawi N, Thewaini AJ 1969. Non-agglutinable vibrios isolated in the 1966 epidemic of cholera in Iraq. Bull WHO 40: 163-166.
  • Gonzalez BC, Villanueva Z, Gutierrez CL, Figueroa P, Giono CS, Velazquez VL 1993. Cambios en la epidemiología mundial del cólera. Difusión de Vibrio cholerae no O1, O139. Bol Cólera/Diarreas Infecciosas 3: 419.
  • Gutiérrez-Cogio L 1995. Variación de las cepas de Vibrio cholerae aisladas en la República Mexicana entre 1991 y 1995. Epidemiología 12: 1-2.
  • Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST 1994. Bergey's manual of determinative bacteriology, p. 273-274. 9th ed., Williams & Wilkins, Baltimore, U.S.A. Kamal AM 1971. Outbreak of gastroenteritis by nonagglutinable (NAG) vibrios in the Republic of Sudan. J Egypt Public Health Assoc 46: 125-173.
  • McIntyre OR, Feeley JC, Greenough WB III, Benenson AS, Hassan SI, Saad A 1965. Diarrhea caused by non-cholera vibrios. Am J Trop Med Hyg 14: 412-418.
  • Mhalu FS, Mmari PW, Ijumba J 1979. Rapid emergence of El Tor Vibrio cholerae resistant to antimicrobial agents during first six months of fourth cholera epidemic in Tanzania. Lancet i: 345-347.
  • Morris JG Jr 1990. Non-O group 1 Vibrio cholerae: a look at the epidemiology of an occasional pathogen. Epidemiol Rev 12: 179-191.
  • Mukhopadhyay AK, Saha PK, Garg S, Bhattacharya SK, Shimada T, Takeda T, Takeda Y, Nair GB 1995. Distribution and virulence of Vibrio cholerae belonging to serogroups other than O1 and O139: a nation wide survey. Epidemiol Infect 114: 65-70.
  • NCCLS-National Committee for Clinical Laboratory Standards 1988. Performance standards for antimicrobial disk susceptibility tests k, de. 4, M2-T4; 8: 75-87. PAHO-Pan-American Health Organization 1995. Cholera in the Americas. Epidemiol Bull 16: 11-13.
  • Ramamurthy T, Garg S, Sharma R, Bhattacharya SK, Nair GB, Shimada T, Takeda T, Karasawa T, Kurazano H, Pal A, Takeda Y 1993. Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India [letter]. Lancet 341: 703-704.
  • Rodier J 1990. Análisis de las aguas. Aguas naturales, aguas residuales y agua de mar, p. 476-478, 2da. reimpresión, Ediciones Omega, S.A., Barcelona, Espańa.
  • Sakazaki R, Donovan JT 1984. Serology and epidemiology of V. cholerae and V. mimicus Meth Microbiol 16: 271-289.
  • Sanyal SC 1992. Epidemiology and pathogenicity of non-O1 Vibrio species and related organisms, p. 57-67. In D Barua, WB III Greenough (eds), Cholera, Plenum Medical Book Company, New York.
  • Shimada T, Arakawa E, Itoh K, Okitsu T, Matsushima A, Asai Y, Yamai S, Nakazato T, Nair GB, Albert MJ, Takeda Y 1994. Extended serotyping scheme for V. cholerae Curr Microbiol 28: 175-178.
  • Shimada T, Nair GB, Deb BC, Albert MJ, Sack RB, Takeda Y 1993. Outbreaks of Vibrio cholerae non-O1 in India and Bangladesh [letter]. Lancet 341: 1347. Spira WM, Ahmed QS 1981. Gauze filtration and enrichment procedures for recovery of Vibrio cholerae from contaminated waters. Appl Environ Microbiol 42: 730-733.
  • Threlfall EJ, Rowe B 1982. Vibrio cholerae El Tor acquires plasmied-encoded resistance to gentamicin. Lancet i: 42.
  • Valdespino Gómez JL 1994. Cólera, p.169-178. In JL Valdespino Gómez, O Velasco Castrejón, A Escobar Gutierrez, A Del Río Zolezzi, S Ibańez Bernal, C Magos López (eds) Enfermedades Tropicales en México. Diagnóstico, tratamiento y distribución geográfica Instituto Nacional de Diagnóstico y Referencia Epidemiológicos, México, D.F.
  • WHO 1993. Epidemic diarrhea due to Vibrio cholerae non-O1. Wkly Epidemiol Rec 68: 141-142.

Publication Dates

  • Publication in this collection
    08 Oct 1998
  • Date of issue
    Jan 1998

History

  • Received
    05 Mar 1997
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