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 ~  Abstract
 ~ Introduction
 ~ Subjects and Methods
 ~ Results
 ~ Discussion
 ~ Conclusions
 ~  References
 ~  Article Tables

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  Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 38  |  Issue : 1  |  Page : 101-108
 

Prevalence and antimicrobial profile of Shigella isolates in a tertiary care hospital of North Karnataka: A 12-year study


1 Department of Microbiology, SDMCMSH, Dharwad, Karnataka, India
2 ICMR-National Institute of Cholera and Enteric Diseases and Officer-in-Charge, ICMR-Virus Unit, Kolkata, West Bengal, India

Date of Submission16-Mar-2020
Date of Decision18-May-2020
Date of Acceptance12-Jun-2020
Date of Web Publication25-Jul-2020

Correspondence Address:
Dr. Deepa R Hanamaraddi
Department of Microbiology, SDMCMSH, Dharwad, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_20_107

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 ~ Abstract 


Context: Shigella is a common cause of bacillary dysentery. Although it is reported worldwide, the majority of the infections are seen in developing countries with Shigella flexneri being the most common isolate. Prevalence of Shigella species and their antibiotic susceptibility profiles vary according to geographic area and season. Aims: In the present study, the epidemiology and antimicrobial profile of Shigella from stool samples received at our hospital for a period of 12 years (January 2006 to December 2017) was evaluated. Subjects and Methods: A total of 4578 stool samples were collected from the cases of acute gastroenteritis and diarrhoea. Samples were processed for culture and sensitivity according to standard microbiological techniques. The presumptive identification of Shigella species was done using standard conventional biochemical tests and confirmed using antisera. Results: A total of 189 (4.2%) samples yielded Shigella spp. Isolation of Shigella spp. were more frequent from males (58.2%). S. flexneri was the commonest species isolated (47.6%) followed by Shigella sonnei(11.6%), Shigella dysenteriae (4.2%) and Shigella boydii (2.1%). Non-typeable Shigella was commonly recovered. The isolates showed high resistance to ampicillin (76.7%) and co-trimoxazole (75%) while highest susceptibility was observed to ceftriaxone (79.2%). Conclusions: S. flexneri was the most prevalent species isolated at this centre. Shigella isolates from the study showed alarming resistance to recommended antibiotics. Non-typeable Shigella accounted for 34.4% isolates. Molecular discrimination between Shigella and Escherichia coli is essential.


Keywords: Shigella, Shigella flexneri, non-typeable Shigella


How to cite this article:
Jain PA, Kulkarni R D, Dutta S, Ganavali AS, Kalabhavi AS, Shetty PC, Shubhada C, Hosamani MA, Appannanavar SB, Hanamaraddi DR. Prevalence and antimicrobial profile of Shigella isolates in a tertiary care hospital of North Karnataka: A 12-year study. Indian J Med Microbiol 2020;38:101-8

How to cite this URL:
Jain PA, Kulkarni R D, Dutta S, Ganavali AS, Kalabhavi AS, Shetty PC, Shubhada C, Hosamani MA, Appannanavar SB, Hanamaraddi DR. Prevalence and antimicrobial profile of Shigella isolates in a tertiary care hospital of North Karnataka: A 12-year study. Indian J Med Microbiol [serial online] 2020 [cited 2020 Aug 7];38:101-8. Available from: http://www.ijmm.org/text.asp?2020/38/1/101/290682





 ~ Introduction Top


The genus Shigella is a group of Gram-negative non-spore-forming bacilli belonging to the family Enterobacteriaceae and is further divided into four species, namely, Shigella dysenteriae, Shigella flexneri, Shigella boydii and Shigella sonnei. Shigella spp. cause mild diarrhoea to fulminant dysentery. Shigellosis commonly causes high morbidity and mortality in children <5 years of age in developing countries. Shigellosis is seen in both endemic and epidemic forms worldwide. The lack of safe water, poor hygiene, close personal contact and malnutrition play an important role in the transmission of Shigella.[1] Rainfall and temperature also contribute to the endemicity of shigellosis.[2]

The primary mode of transmission of this highly infectious pathogen is faeco-oral and as low as 10–100 bacilli may initiate a clinical infection.[3]Shigella colonises and invades the intestinal epithelium leading to disruption of colonic mucosa. Loose motions, abdominal cramps, fever, tenesmus are the cardinal features of shigellosis.[4]

True prevalence of Shigella cannot be estimated reliably as most infections are mild and self-limiting, not needing medical attention or laboratory evaluation.[5] In addition, the sensitivity of culture is low because of low bacterial load or prior antibiotic therapy as well as poor transportation of samples.[6] As per reports, estimated annual mortality of 35,000–40,000 is noted globally in both under five and older than 5 years age groups.[7],[8] The number of Shigella-related deaths in Asia has substantially decreased due to current non-specific interventions, including measles vaccination, Vitamin A supplementation and improved nutrition.[8]

S. flexneri is prevalent in developing countries from Asia and Africa and S. sonnei is reported mainly from industrialised countries.[9],[10]S. flexneri was found to be the most common species isolated among the Asian countries (68%), except in Thailand, where S. sonnei was the most common.[10],[11] Studies from India also showed S. flexneri being the most common serogroup (60%–74.7%).[4],[10],[11] It is observed that S. flexneri and S. sonnei are responsible for endemic disease in India and S. dysenteriae causes epidemics or outbreaks at different intervals.[12] Similar distribution of Shigella species has been noted from Karnataka.[13]

Shigella rapidly acquires antibiotic resistance. The first report of resistance to sulphonamide in Shigella came from Japan in 1940.[14] Because of the development of resistance to chloramphenicol, ampicillin, cotrimoxazole and nalidixic acid by 1990, ciprofloxacin was recommended as the drug of choice for empiric treatment of shigellosis. Due to the injudicious use of ciprofloxacin, resistance emerged against this antibiotic as well.[14] The WHO now recommends ceftriaxone, pivmecillinam and azithromycin as alternative drugs to fluoroquinolone-resistant Shigella. Resistance to these recommended drugs has also been observed in African and Asian countries.[15]

Prevalence of Shigella species and their antibiotic susceptibility profile is known to vary according to geographical area and season.[4] Therefore, evaluating the prevalence of Shigella species and their antibiogram in a given geographical area can help to provide evidence-based guidance for the empirical therapy of the disease. We, therefore, reviewed the prevalence of Shigella species and their antimicrobial profile at our centre from stool samples over a period of 12 years (January 2006 to December 2017).


 ~ Subjects and Methods Top


From January 2006 to December 2017, over a period of 12 years, 4578 stool samples were collected from the cases of acute gastroenteritis and diarrhoea. The specimens were inoculated on blood agar, MacConkey's agar, xylose-lysine deoxycholate (XLD) agar and in selenite-F enrichment broth. After 6 h of incubation in selenite-F broth, subculture was done on MacConkey's agar and XLD. Suspected Shigella colonies were identified by using standard biochemical identification tests.[16] Confirmation of Shigella isolates was done using slide agglutination with specific anti-sera (Denka-Seiken, Japan). Antimicrobial susceptibility was tested by Kirby-Bauer disk diffusion technique as per the CLSI (Clinical and Laboratory Standards Institute) guidelines using following disks–ampicillin (10 μg), cotrimoxazole (25 μg), ciprofloxacin (5 μg) and ceftriaxone (30 μg) (HiMedia Laboratories, India).[8],[17] Some of the isolates were sent to National Institute of Cholera and Enteric Disease (NICED), Kolkata, for confirmation.


 ~ Results Top


A total of 4578 stool samples were received at the Bacteriology Laboratory for culture and sensitivity over a period of 12 years from 2006 to 2017 and 189 (4.1%) samples yielded Shigella isolates. Of the 189 isolates, 110 (58.2%) were from males, while 79 (41.8%) were from female patients [Table 1]. Of 189 Shigella isolates, 110 Shigella isolates were confirmed as Shigella species from NICED, Kolkatta.
Table 1: Species and Sex wise distribution of cases

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As shown in [Table 2], age-wise distribution of shigellosis cases is shown. The age of the youngest case was 1 year, while that of the eldest was 75 years. Maximum numbers of isolates were recovered from the age group of 16–60 years (109/189; 57.7%) and the age group of 6–16 years gave 6.3% isolates. The overall prevalence of Shigella spp. in the stool samples received at our centre was 4.1% (n = 189). The highest isolation of Shigella was seen in the year 2015 (24.9%), followed by in 2013 (16.4%).
Table 2: Age-wise distribution of cases

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Species diversity

Among 189 Shigella isolates, 124 (65.6%) isolates were identified to the species level. From our isolates, 65 (34.4%) isolates were phenotypically identified as Shigella; however, these isolates did not show agglutination with Shigella antisera and, therefore, were grouped as non-typeable or non-agglutinable Shigella [Table 3]. Of 124 speciated Shigella, the most common isolate was S. flexneri and the least common was S. boydii.
Table 3: Year-wise distribution of cases

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Seasonal variation in isolation

The isolation frequency showed seasonal variation, and the highest isolation was noted during the monsoon (86/189) followed by winter (59/189). Summer recorded the least isolations (44/189). Isolation of S. flexneri was seen round the year with peaks in the months of April, July, August and November. Isolation of S. flexneri was highest in the year 2015 (n = 21), followed by 2013 (n = 13) and 2016 (n = 13). In 2015, the highest isolation was noted in June. Isolation of S. sonnei was highest in 2015 (n = 10) with uniform distribution throughout the year. There was no specific seasonal variation in S. boydii and S. dysenteriae isolations. Among the non-typeable Shigella isolation was highest in 2012 (n = 15), followed by in 2015 (n = 13) [Table 4].
Table 4: Seasonal variation

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Antimicrobial profile

Resistance shown by the isolates to ampicillin, cotrimoxazole, ciprofloxacin and ceftriaxone was 76.7%, 75%, 51.2% and 20.8%, respectively. The isolates showed the highest susceptibility to ceftriaxone (79.2%), followed by ciprofloxacin (48.7%) [Table 5].
Table 5: Antibiogram

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 ~ Discussion Top


Shigella infections are an important cause of diarrhoea or dysentery globally. Shigella episodes all over the world have been estimated to be 164.7 million annually. A huge proportion of these episodes (163.2 million) affect developing countries causing 1.1 million deaths. In comparison, only 1.5 million Shigella episodes are reported from industrialised countries. Children under five years of age face the biggest brunt of the disease as 69% of episodes and 61% of deaths are seen in children.[1],[18] The present study discusses Shigella isolations from 2006 to 2017, a period of 12 years at a tertiary care institute located in North Karnataka. This is the first report on the prevalence of shigellosis from a tertiary care centre of Hubli-Dharwad region of Karnataka.

Culture is the gold standard for the diagnosis of shigellosis. A total of 4578 stool samples were received for culture and sensitivity at our laboratory during the study period from which 189 Shigella isolates belonging to all the four species and non-typeable Shigella were recovered. The youngest case was 1 year, while the eldest was 75 years of age.

Children under five, especially in developing countries, are most vulnerable to Shigella morbidity and mortality. Kotloff et al. reported that 69% of all shigellosis were observed in children, <5 years of age.[1] They also estimated that a total of 11,316,260 episodes of shigellosis occur each year in children under5 years in the developing world.[1] Mamatha et al. in their review of 68 cases, reported 60.2% cases below 5 years of age.[19] Ghavam et al. isolated Shigella from 64.1% of cases in children <5 years of age.[20]

In the present study, 18.5% of the cases belonged to under-five age groups (35/189) and the highest isolation of Shigella was seen in the age group ranging from 16 to 60 years (109/189; 57.7%). Lower prevalence of Shigella infections in children under five may be attributed to the hierarchy of the hospital. This being a tertiary care hospital, only the severe cases from the area might have been referred to this hospital.

The prevalence of shigellosis varies from place to place. In the present study, male patients (58.2%) outnumbered female patients. The male-to-female ratio as observed by Mamatha et al., in a study over 6 years was 3:1.[19] Similar observations were note in other studies.[6],[13],[20],[21],[22]

Shigella isolations in the present work were seen round the year with two seasonal peaks. The first peak was during the monsoon months, i.e., June to August and the second peak was observed in November. Though November ushers the winter season, Dharwad district of North Karnataka receives 'retreat monsoon' during November and this could be a reason for the peak observed in this month.[23],[24] Studies from Bangladesh showed the highest isolation at the beginning of monsoon months and second peak in winter.[25]

From the stool samples received at our laboratory for culture and sensitivity 4.1% samples yielded Shigella. A similar isolation rate of Shigella has been reported by other workers.[4],[13],[25] Isolation rates vary from 1% to 15% in different parts of India. Isolation rates are commonly found to be higher in paediatric age group.[26],[27]

In this study, we found S. flexneri to be the most common species (90/189; 47.6%) followed by S. sonnei (22/189, 11.6%), S. dysenteriae (8/189; 4.2%) and S. boydii (4/189; 2.1%). Reports from various parts of India showed a similar pattern of species distribution. Reports from Karnataka also show the predominance of S. flexneri followed by S. sonnei.[13],[23] In contrast to this observation, S. dysenteriae isolations (48.83%) were higher than S. flexneri (32.55%) in a report by Prabhurajeshwar et al.[21] This, however, could be a smouldering outbreak rather than true endemicity. von Seidlein et al., conducted a multicentric study on Shigella episodes in Asian countries and found S. flexneri to be the predominant species (68%) except in Thailand, where S. sonnei was most common (85%).[11] Chang et al., meta-analysed 131 articles pertaining to Shigella episodes and showed that 76.2% of Shigella episodes were caused by S. flexneri in most geographic regions of mainland China followed by S. sonnei (21.3%).[18] However, in India, as far as outbreaks are concerned, S. dysenteriae is more common than other species.[4]

S. sonnei was the second most common isolate from our study. With improvements in hygiene, sanitation and better quality drinking water supply, other species of Shigella are on decline from the developing countries. In fact, from the developed countries, S. sonnei is the most common isolate.

In the West, there is a concern about patients returning from India because of the acquisition of highly drug-resistant strains. Therefore, in the Western world, different empirical antibiotic choice is contemplated for patients returning from India.[28] Although S. flexneri is the most common species in India, the travellers returning from India often show S. sonnei infections. It is highly likely that the European travellers are exposed to the 'developed or affluent India', unlike the general Indian population. This, therefore, predisposes them to acquire S. sonnei rather than S. flexneri.[29]

In developing countries, S. dysenteriae is associated mainly with outbreaks, but isolation rates from endemic cases are low.[4] A report from Gulbarga in north Karnataka showed higher isolation of S. dysenteriae (48.3%). The duration of this study was approximately 10 months, and it included only paediatric patients. The duration of 10 months does not qualify to call it an outbreak and this could be a smoldering outbreak over a period of 10 months.[21]

S. boydii, though uncommon in other Asian countries, was very common (23%) in cases from Bangladesh.[25] In the present study, S. boydii was the least common isolate accounting for 2.1% of all the Shigella isolates.

Many Shigella isolates from our study were non-typeable (34.4%; 65/189). A few other studies have reported non-typeable Shigella; however, the proportion of non-typeable Shigella in this study is higher compared to other reports.[30]

Though enteroinvasive Escherichia coli (EIEC) and Shigella are phenotypically indistinguishable, EIEC are rarely encountered in dysentery cases.[31] We, therefore, have placed these isolates under non-typeable Shigella group. EIEC or atypical E. coli and Shigella produce clinically identical intestinal infection. Moreover, to discriminate between atypical E. coli and Shigella, even by molecular methods is beyond the scope of most diagnostic laboratories across the world. Both species are profoundly homogenous on DNA study.[31] PCR targeting iapH gene has been used to identify Shigella in stool samples. This PCR, however, cannot differentiate Shigella and E. coli.[6],[22]

The query is, does atypical E. coli have the potential to produce outbreaks, epidemics and endemicity similar to Shigella? Researchers are reluctant to deal with E. coli because of their commensal nature and the enormity of their serotypes. It is, therefore, important to develop some easier and implementable techniques to discriminate between Shigella and atypical E. coli for better characterisation and investigating their epidemiological importance. Radhika et al., 2014 have reported a Shigella genus-specific PCR targeting the ipaH1 gene that does not amplify the standard strain of E. coli. This test needs further exploration. It is certainly essential because GI infections are very important cause of morbidity and mortality, especially in children of the developing world.[32]

Shigellosis is a very important public health problem, with an increase in drug resistance, the treatment options are expensive and difficult; therefore, vaccine against Shigella is the need of the hour.[33],[34] The studies so far have shown that the vaccines are group-specific and not serotype-specific. A comprehensive and current understanding of the prevalent Shigella species and serotypes is essential for the development of an effective vaccine.[35] Currently, though several strategies have been used to develop vaccines for shigellosis, only one live bivalent S. flexneri 2a and S. sonnei vaccine is licensed in China, which is serotype-specific.[36],[37] With the increasing presence of non-typeable Shigella, the development of vaccines may face additional challenges.

In Shigella, multidrug resistance is commonly reported all over the world.[4] Centre for Disease Control in 2013 has categorized Shigella infections as a serious threat because of drug resistance.[20] Although shigellosis is a self-limiting disease, WHO guidelines suggest antibiotic therapy to reduce the severity, death and carriage of organisms. Antibiotics, therefore, help to curb the spread of Shigella in the community.[38] Resistance to ciprofloxacin, βlactam antibiotics or plasmid-mediated azithromycin resistance is of high concern.[39],[40] Antibiotic susceptibility to ampicillin, ceftriaxone, ciprofloxacin and cotrimoxazole was performed as recommended by the WHO during this work.[15]

Sulphonamide resistance was observed in Shigella isolates in the late 1940s and therefore, tetracycline and chloramphenicol were recommended as alternative antibiotics.[41] Shigella developed resistance to these antibiotics that led to the inclusion of ampicillin and cotrimoxazole in the treatment of shigellosis. These antibiotics were opted out in the 1980s as high resistance to these agents was noted during the Shigella epidemics from eastern India. From 2010 resistance to ampicillin observed by various workers was always above 65%.[26] The concept of drug of choice for shigellosis seems to be fading because of the changing pattern of antimicrobial susceptibilities among Shigella isolates. The problem of resistance and its changing trend is largely related to the commoner isolates like S. dysenteriae and S. flexneri.[4]

A total of 79.5% S. flexneri isolates in the present study were resistant to ampicillin. The other species – S. dysenteriae (80%), S. boydii (75%) and S. species (81.8%) showed comparable resistance to ampicillin. However, S. sonnei with 33.3% resistance, showed the least resistance to ampicillin. We observed considerable variation in ampicillin resistance from 100% to 25% throughout the study without any specific trend. Studies from coastal Karnataka have observed 100% resistance to ampicillin.[13],[19],[42] Reports from Gulbarga, North Karnataka showed 100% resistance to ampicillin in all four species.[21] The non-typeable Shigella also showed higher resistance to ampicillin (81.8%).

We have noted an overall resistance of 70.9% to cotrimoxazole. For S. flexneri it was 70.4% while in S. dysenteriae, S. sonnei and S. boydii, it was between 50% and 66.7%. Other studies have recorded up to 89% resistance to cotrimoxazole.[4],[13],[21] In the present study, the susceptibility to cotrimoxazole did not show any specific trend with rising resistance from 2010 onwards.

Nalidixic acid was the most commonly used quinolone in the treatment of Shigella infections earlier. Resistance to nalidixic acid among Shigella species was observed from the 1990s and it became outdated for the treatment of shigellosis in India.[4],[21] Subsequently, ciprofloxacin, a derivative of nalidixic acid, became the drug of choice.[43] However, resistance to ciprofloxacin was reported soon.[43],[44],[45],[46] Mamatha and Rituparna showed an increase in resistance to ciprofloxacin from 30 to 87% from the year 2006 to the year 2011.[13] Curiously, the resistance was noted to be higher in isolates from children.[47] Overall resistance Shigella isolates in the present study to ciprofloxacin were 56.2%. Susceptibility to ciprofloxacin varied throughout the 12 years study period reaching highest, i.e., 84.6% in 2015. In S. flexneri, 54.2% of isolates were resistant to ciprofloxacin. As we encountered only four S. boydii it is not appropriate to comment about their susceptibility; however, three of these four isolates were sensitive to ciprofloxacin. It is reported by other workers that antimicrobial resistance is higher among S. dysenteriae type 1 and S. flexneri compared to other serogroups.[48] We could subject only five of the eight S. dysenteriae isolates to antibiotic susceptibility test and all were resistant to ciprofloxacin.

In 2013, the WHO recommended ceftriaxone, pivmecillinam and azithromycin as alternative drugs for fluoroquinolone-resistant Shigella.[15] However prevalence of 14.2% resistance to ceftriaxone, 22.6% to pivmecillinam and 6.2% to azithromycin has been reported during 2010–2012.[49]

In 2016, the WHO recommended ceftriaxone as an alternative drug only to be used when local Shigella isolates show resistance to ciprofloxacin.[4] With the high proportion of drug-resistant isolates reported from various studies, pivmecillinam and ceftriaxone remain the best choices in the treatment of multidrug-resistant Shigella.[4] In this study, 78.4%. Shigella were sensitive to ceftriaxone. The resistance to ceftriaxone over the study period started rising after 2014 and went from 11.0% to 30.7% in 2016. S. flexneri showed 86.6% susceptibility to ceftriaxone, followed by S. sonnei (77.8%). Out of 8S. dysenteriae, 4 isolates were sensitive to ceftriaxone. Similarly, 2 out of 4 S. boydii were sensitive to ceftriaxone. A study from Kolkata reported that 94% of MDR Shigella isolates were sensitive to ceftriaxone.[50],[51] Studies from Karnataka also showed high susceptibility to ceftriaxone.[13],[23] However, Taneja and Mewar showed increasing resistance to cephalosporins from 2001 to 2005.[4] The emergence of resistance to ceftriaxone thus needs attention in the management of shigellosis. Shigella is also known to carry multiple drug-resistant genes compared to other Enterobacteriaceae members.[4]

Azithromycin was considered to be the last choice for the treatment of bacillary dysentery. Decreased susceptibility to azithromycin was reported in the recent years from worldwide. Resistance to azithromycin by Shigella is thought to be plasmid-mediated due to the acquisition of mphA and ermB genes in the microbiota. After 2000, the resistance to azithromycin became evident due to increased usage of azithromycin. Increase in resistance to fluoroquinolones and third-generation cephalosporin, azithromycin was used as the last option. It becomes of utmost important to periodically check for MIC and disc susceptibility breakpoints for azithromycin resistant Shigella strains.[52],[53]

Azithromycin resistance among Shigella species was not common in the 18-year period between 1994 and 2012 in the South East Asian countries as shown by Darton et al., and the increase in multidrug-resistant isolates will inevitably lead to increase in the use of azithromycin.[52]

Khan et al. in their study, showed the efficacy of azithromycin in the treatment of shigellosis. Therapy was bacteriologically successful in 32 (94%) patients receiving azithromycin and in 36 (100%) patients receiving ciprofloxacin. The study showed Azithromycin as effective in the treatment of moderate-to-severe shigellosis caused by multidrug-resistant Shigella strains.[54]

In one of the studies done by Salah et al., S. flexneri showed a high resistance pattern to the oral antibiotics such as ampicillin (85%), co-trimoxazole (78%), tetracycline (50%) (Unpublished data) and to azithromycin (42%).[55]

Data on azithromycin resistance in Shigella species are few. A recent report from Bangladesh showed 16% of Shigella isolates were resistant to azithromycin and 62% showed intermediate resistance as per Clinical Laboratory Standards Institute breakpoints recommended for streptococci (>1 mg/L, resistant; <0.25 mg/L, susceptible). The MIC90 (MIC at which 90% are susceptible) of 8 mg/L showed by the microorganisms was within the normal range of MICs for this microorganism; no isolate had an azithromycin MIC > 24 mg/L, which suggests that none had acquired resistance to azithromycin. Surveillance for resistance to azithromycin in Shigella species requires specific breakpoints for this species.[56]

As azithromycin is recommended for the treatment of multidrug-resistant Shigella infection, the susceptibility of these isolates to azithromycin should be periodically tested. Treatment of Shigella infection with oral antibiotics continues to be challenging, as multidrug resistance continues to exist. To determine the sensitivity patterns of azithromycin laboratories must exert maximum efforts to meet the challenges.


 ~ Conclusions Top


There is a need to update the guidelines for the treatment of Shigellosis in developing countries. Shigellosis occurs predominantly in developing countries due to overcrowding and poor sanitation. Infants, non-breast-fed children, children recovering from measles, malnourished children and adults older than 50 years have a more severe illness and a greater risk of death (WHO guidelines, 2016). Because of the limited availability of effective antimicrobial agent choice, emphatic and rigid guidelines are essential with a strong will to follow the strategies assiduously.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 ~ References Top

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2004 - Indian Journal of Medical Microbiology
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