Epidemiology and Antibiotic Susceptibility of Vibrio cholerae Associated with the 2017 Outbreak in Kasese district

doi:10.21203/rs.2.11224/v2

Download PDF

Research article

Epidemiology and Antibiotic Susceptibility of Vibrio cholerae Associated with the 2017 Outbreak in Kasese district

https://doi.org/10.21203/rs.2.11224/v2

This work is licensed under a CC BY 4.0 License

Journal Publication

published 29 Oct, 2019

Read the published version in BMC Public Health →

You are reading this older preprint version

Read the latest preprint version →

Background Cholera has continued to be a global threat to public health and a key indicator of lack of social development in developing countries. This report summarizes findings from the epidemiologic investigation, which aimed at identifying the mode of transmission and antibiotic susceptibility patterns of the Vibrio cholerae isolated in Kasese district, Uganda. Materials and methods This was a descriptive cross-sectional study to describe the epidemiology of the 2017 cholera outbreak in Kasese district. Rectal swabs were collected from 69 suspected case-persons and cultured on Thiosulphate-Citrate-Bile-Salts Sucrose (TCBS™; SEIKEN Japan) agar and incubated at 370C for 18-24 hours. The isolates were serotyped with polyvalent 01 antiserum and monovalent serotype Inaba and Ogawa antisera (Denka Seiken, Tokyo, Japan) to determine which serotype was responsible for the outbreak. Antimicrobial susceptibility testing was performed using the Kirby-Bauer disk diffusion method on Mueller-Hinton agar. Results A total of 222 cases were recorded in the Kasese District outbreak between the month of September 2017 and January 2018 with the case fatality rate (CFR) of 1.4%. Children below the age of 14 years contributed the biggest proportion of the cases (70%) and out of these, 33% were aged below five years. Antibiotic susceptibility using Kirby-Bauer disc diffusion method showed 100% resistance to Ampicillin and over 50% were resistant to trimethoprim/sulfamethoxazole whereas gentamicin showed 100% susceptibility. The general trend also showed increased susceptibility to combination therapy as opposed to mono-therapy.

Infectious Diseases

Health Economics & Outcomes Research

Health Policy

Cholera

antibiotic resistance

epidemiology

environment

Cholera has continued to be a global threat to public health and a key indicator of lack of social development (1, 2). The World Health Organization (WHO) estimates that 3–5 million annual cases of cholera occur worldwide, resulting in 100,000–120,000 deaths (3). Since its introduction to Africa during the seventh cholera pandemic in 1970, Vibrio cholerae caused regular vast epidemics across the continent with cumulative 3,762,902 case-notifications (4). In 2013 alone, 22 African countries reported 56,329 cholera cases. However, these numbers are substantially underestimated due to poorly functioning national epidemiological and laboratory surveillance systems, which are not able to detect the majority of mild disease presentations (4). Emergencies often have a direct impact on the health systems and public health systems of an affected region or country, particularly in resource-constrained areas (5, 6). Factors that may lead to outbreaks in endemic areas include wars, civil unrests, flooding, earthquakes, landslide, poor sanitation and improper refuse dumping, open defecation and slumps (7). The mode of transmission of Cholera is through fecal contamination of food or water. Transmission is therefore closely associated to poor environmental management due to water and sanitation issues (1, 2).

In Uganda, which is one of the 51 endemic countries, cholera outbreaks occur mainly along the western border with Democratic Republic of Congo (DRC), in the Karamoja region to the north, Mbale in the Eastern Region and in the slums of Kampala City (8). Kasese district is affected by regular cholera epidemics. The different Serotypes and biotypes have been reported in the previous studies in Uganda (9). However, antibiotic susceptibilities have not been determined. Kasese District has a hilly terrain; hence many areas are supplied by gravitational water flow schemes (GWFS). Poor hygiene and sanitation conditions and regular flooding of the low lands usually create an ideal environment for disease to spread. Consequently, the district is prone to waterborne diseases, including cholera (10) Kasese suffers frequent annual outbreaks of cholera and in each outbreak, death of a case is the usual trigger for the surveillance activities. On 2^nd October 2017, the Ministry of Health in Uganda issued an alert of a cholera outbreak in Kasese District. This report summarizes findings from the epidemiologic investigation, which aimed at identifying the mode of transmission and antibiotic susceptibility patterns of the Vibrio cholerae isolated in Kasese district.

Study design and study area

This was a descriptive cross-sectional study carried out between September 2017 and February 2018 to describe the epidemiology of the 2017 cholera outbreak in Kasese district, Uganda (Fig. 1). Kasese District is located along the equator in the western part of Uganda and it is bordered by Kabarole District to the north, Kamwenge District to the east, Rubirizi District to the south, and the Democratic Republic of the Congo to the west. Kasese district has 20 rural sub-counties and 4 towns with 115 parishes/wards and 656 villages. The district has a population of 757,269 people, 134,037 being children below 5 years and a majority of the population living in rural areas. The leading cause of morbidity is malaria (30%) and acute diarrhea which is also a major presenting symptom for cholera, is the third most important cause of Morbidity (11).

Study population and sampling

The study population comprised of both adults and children suspected to be suffering from cholera admitted in the isolation wards in Kagando hospital and Bwera hospital. A case of cholera was defined according to the WHO standard case definition: if cholera is not known to be present in the area, a case of cholera is in a patient ≥5 years with severe dehydration or death from acute watery diarrhea, while during a cholera epidemic, every patients ≥5 years with acute watery diarrhea and/or vomiting is considered as a case (12). In the community, the patients who were discharged from the isolation wars or their parents/guardians formed the study population. Consecutive sampling was carried out throughout the outbreak season until the time when the epidemic was controlled. Sample size calculation was not applicable.

Data collection

A list of discharged patients was obtained from the isolation units of Bwera hospital and Kagando hospital and the individuals were followed to the community where they live. A total of 222 patients were recorded in the discharge book some of whom were children and these were followed to the community. We obtained telephone contacts of the care takers and worked with community health workers also referred to as Village Health Teams (VHTs) to locate the cases. Key questions on symptomatology and environment were asked. Major symptoms looked out for included acute diarrhea, vomiting and abdominal cramps. Environmental assessment was carried out using an environmental checklist. The key elements of the environmental checklist included; safe water, food safety, sanitation and hygiene, personal, family and school hygiene, municipal water supplies, other water supplies, solid waste disposal, disposal of excreta and treatment of waste water. We also took GPS points of the homes of the cases and pictures of potential source infection (Fig. 1).

Laboratory detection of Vibrio cholerae

Self-collected rectal swabs from suspected case-persons were transported to the laboratory in alkaline peptone water medium for culture and sensitivity. ‘Case-persons’ is used in this study to mean persons with signs and symptoms matching the WHO standard case definition for cholera (World Health Organization, 2004)(12). The samples were cultured on Thiosulphate-Citrate-Bile-Salts Sucrose (TCBS™; SEIKEN Japan) agar and incubated at 37⁰C for 18-24 hours. The isolates were serotyped with polyvalent 01 antiserum and monovalent serotype Inaba and Ogawa antisera (Denka Seiken, Tokyo, Japan). Rectal swabs were collected from 71 participants and antibiotic susceptibility done in Bwera hospital and Kagando Hospital laboratories.

Antibiotic susceptibility testing

Antimicrobial susceptibility testing was performed using the Kirby-Bauer disk diffusion method on Mueller-Hinton agar. The Escherichia coli reference strain ATCC 25922 was used as a control. Isolates were tested against 7 antimicrobial drugs as follows: ampicillin (10 μg), ciprofloxacin (5 μg), chloramphenicol (30μg), gentamycin (30μg), nalidixic acid (30μg), sulfamethoxazole/trimethoprim (1.25 μg + 23.75 μg) and tetracycline (30μg) (all Oxoid, United Kingdom). Zones of inhibition were interpreted according to the 2014 Clinical and Laboratory Standards Institute (CLSI) guidelines as resistant and susceptible (13).

Potential sources of bias

Recall bias was the most common potential confounder as recollection of previous events might have been difficult for our respondents. However the authors tried to minimize this by administering the questionnaires during the outbreak season to benefit from fresh memories.

Ethical considerations

Ethical approval was obtained from the Makerere University School of Biomedical Sciences Higher Degrees Research and Ethics committee (SBS-292). Written informed consent was obtained from all study participants. Consent from parents/guardians of participants below 18 years was sought and ascent was obtained from all minors who took part in this study. Participation was voluntary.

Data management and presentation

Data was checked for completeness to avoid cases of missing data and entered in excel. The variables of interest collected include; age sex, date of onset of symptoms, date of admission, duration of hospitalization, outcome and laboratory results, recovery and death. Cleaned data was exported to STATA v14 for analysis in time, place and person and presented in form of Tables and Figures.

Epidemiological description of the 2017 outbreak

A total of 222 cases were recorded in the Kasese District outbreak between the month of September 2017 and January 2018 with the case fatality rate (CFR) of 1.4%. By the time the outbreak started, the laboratory lacked necessary supplies to confirm the cases. The patients who died were two females aged 17 and 30 years and one male aged 60 years. The index case reported onset of symptoms on 23^rd September was admitted on 24^th September, the number of cases came to a peak at 87 in the epidemiologic week 39 and the last case was admitted in the epidemiologic week 49 (Fig. 2) before a drastic reduction in the epidemiologic week 41 due to initiation of the interventions to control the disease by the district response team. Few cases continued to be reported in a lower frequency until the outbreak was fully contained by the 8^th of January 2018. The median age of the cases was 8 years and ranged from 7 months to 75 years. Children below the age of 14 years contributed the biggest proportion of the cases (70%) and out of these, 33% were aged below five years. Katojo primary school had 22 cases among the pupils and their latrine was washed away by the floods into river. The average hospital stay for the admitted cases was 4 days.

Symptomatology and clinical picture

Questionnaires were administered to a total of 75 participants who were either the cases or a relatives to the case. In instances where the case was found dead or when the case was still recovering we opted to interview a relative who was a care taker. For the cases that were clustered in one place, only one case or relative of the case was selected randomly and considered for interviews.

The greatest proportion of the cases (92%) were clinically diagnosed and managed without laboratory confirmation for Cholera. All the cases in this out break presented with diarrhea as the most common symptom (100), followed by vomiting (92%). Abdominal cramps was however present in only 39% of the cases (Table 1).

Environmental conditions in the outbreak area

Environmental assessment of the residences of the cases indicated inadequate water supply, poor sanitary conditions and unsafe disposal of solid waste (Fig. 3). All the three case fatalities were reported to consume untreated surface water with no methods employed to make the water safe for human consumption.

Though we were not able to culture water samples to confirm the source of infection, we hypothesize that the outbreak of the disease was caused by exposure to faecal contaminated water or food, following a series of floods that washed away latrines into water sources in sub-counties of Nyakiyumbu, Bwera and Isango. The most affected villages included; Bunyiswa, Rwehingo, Katholhu, Rusese and Kyanzi.

Other factors responsible for its spread include poor personal hygiene, using contaminated water, poor sanitation as occurs in open defecation, eating food or drinks prepared under unhygienic conditions and poor personal hygiene, especially not washing hands after visiting the toilet.

Water sources and safety

Drinking safe water was not a concern until the time of the outbreak with 49% (37/75) of the homesteads consuming untreated surface water. Only 16% (12/75) of the homesteads reported consuming municipal tap water while the rest, 35% (26/75) consumed borehole water. None of the participants reported boiling drinking water or use of chemi-sterilants before the outbreak period. During the mapping exercise, we did not find any piped (tap) water in the entire outbreak zone and there was only one borehole sited in the whole community. The main source of water was river Kiyanzi which is untreated surface water, visibly turbid with on-going sand mining activities.

Other sanitary conditions in the homes of the cases

Whereas most households in the outbreak area had poor pit latrines, there were rampant cases of open defecation. Most of the pit latrines were unimproved (Fig.4) and some were washed away by heavy floods into the river and this is what sparked of the outbreak. Hand washing facilities were not observed at the pit latrine area a good indication for poor hand hygiene. Most of the toilets and kitchens were built as temporary structures using mad, banana fiber or grass which compromises food hygiene.

Besides the poor management of the human excreta, there was generally poor management of solid waste in the entire community. River banks were the dumping sites for garbage. The cooking areas were not safe for preparation of food and when it rained, the whole area was covered by mud. Most houses of the cases were made of mud walls and most times, especially during flooding, rain water entered the houses.

Table 1: Distribution of cholera cases by person, place, time and diagnosis in Kasese district, 2017

Characteristics	No. cases	percentage
Age group (Years)
<5	25	33
5-14	28	37
15-24	5	7
25-34	6	8
≥ 35	11	15
Sex
Male	41	55
Female	34	45
Source of Drinking water
Untreated open water source/river	37	49
Municipal tap water	12	16
Borehole water	26	35
Duration in isolation unit (days)
1 - 3	43	57
4 - 6	28	37
Above 6	4	5
Symptoms
Diarrhea	75	100
Vomiting	69	92
Abdominal cramps	29	39
Type of diagnosis
Clinical	69	92
Laboratory confirmation	6	8

The most affected people were from Bukonzo West constituency, an area that neighbors the Democratic Republic of Congo. This V. cholerae outbreak was epidemiologically linked to consumption of untreated surface water after heavy flooding leading to a number of pit latrines washing away into the water according to our environmental assessment report and case and/ care taker interviews. Water from this river is consumed without treatment and therefore exposing people to cholera and other water borne diseases.

Antimicrobial susceptibility

Antibiotic susceptibility using Kirby-Bauer disc diffusion method showed 100% resistance to Ampicillin and over 50% were resistant to Trimethoprim/Sulfamethoxazole. Drugs like tetracycline which is among the recommended drugs in the clinical guidelines had close to 50% resistance whereas gentamicin showed 100% susceptibility. In addition, drugs like chloramphenicol and ciprofloxacin showed low resistance rates (11.76% and 5.9%) respectively. The general trend also showed increased susceptibility to combination therapy as opposed to mono-therapy (Fig. 5).

A total of 222 cases were recorded in the 2017 with the case fatality rate (CFR) of 1.4%. This CFR is high because in Uganda, death of a case or two is usually a common trigger to intervention and surveillance activities. The persistently high number of cases reported in the frequent cholera outbreaks in Kasese district with some deaths at least reported during each outbreak may reflect more general problems in access to effective health care (9, 14). Uganda enjoys an international applause in management of emergency outbreaks like Ebola and Marburg due to availability of a fully functional state-of-the-art Public Health Emergency Operating Center and an operational public health emergency response plan (15), but more needs to be done in the case of Cholera (16). Bwera hospital and Kagando hospital, like other hospitals in Uganda, have a small health work force (17) that each time needs to heavily rely on other in-country work force in the emergency situations. Access to effective health care also largely depends on the availability to patients often too ill to walk. Cases were located in areas with unpaved roads (Fig. 6) that could not be accessed by motorized transport means. During the mapping of cases, we went sliding and surviving several falls to access homes of cases. The problem of poorly or unpaved roads though seems to be similar across the resource constrained settings across Africa, Asia and Latin America (18).

Even with the poor road infrastructure, the local district team with the benefit of the previous experience of managing cholera outbreaks quickly and effective responded with awareness messages and active identification of cases. At the time of the outbreak, the laboratory lacked culture media and other necessary supplies necessary to detect and confirm the Cholera cases, at that point, anybody who presented with diarrhea was considered a case. A similar study in Kenya also pointed out similar challenges of supply chain and non-preparedness to respond to cholera outbreaks (19).

Similarly, over 100 people were affected by cholera in the same district in the year 2015 (9). The frequent outbreaks in Kasese district and other parts of Uganda have continued to feed into the high density of cholera cases reported in Sub-Saharan Africa.

Environment and sanitation

Kasese District is a hilly area with vast low lands that suffer frequent flooding. The outbreak of 2017 proceeded heavy flooding that washed toilets into the river in the low land. Consumption of contaminated water has been repeatedly implicated in a similar cholera outbreaks in Kasese (9), other parts of the country like Karamoja in North Eastern Uganda (14) and elsewhere in the world (20-22). Most of the latrines in the affected area were unimproved and this could have encouraged rampant cases of open defecation. While the National Housing and Population census reports that only 10% of the rural population in Uganda lacks access to pit latrines, it also acknowledges that about 58% of the pit latrines are unimproved (23). The quality of latrine facilities needs to be addressed if Kasese is to meet the sanitation SDG targets. Katojo Primary school whose latrine was washed away by the floods also had no hand washing facilities with evidence of open defecation around the latrine which points to the fact that the pupil to stance ratio is higher than the recommended 40:1 (pupil: stance) (24) meaning that the pupils have to queue longer to access the latrine facilities at any given time. Similarly the Uganda national rural school pupil to stance ration has been reported to have increased from 70:1 to 71:1 between 2014 and 2015 (24).

Antibiotic susceptibility

In this study, we report a high resistance to Ampicillin and trimethoprim/sulfamethoxazole and this compares with the findings of other studies (25). We note with great concern the high resistance to tetracycline of over 50% yet it is one of the main antibiotics recommended in the management of Cholera (Fig.5). Several other studies have reported the rise in resistance to tetracycline by V. cholerae (25, 26). The greatest susceptibility was noted in gentamicin and low resistance against ciprofloxacin was recorded. Similar studies have documented that there has been no notable change in the resistance to ciprofloxacin (25). Multi-drug resistance has also been noted in this study. With the emergence of multidrug resistance among V. cholerae isolates, Uganda now faces a double challenge of both control and management of cholera epidemics.

Though we did not culture water to confirm contamination with Vibrio cholerae, we hypothesize that Kasese Cholera outbreak 2017 was caused by exposure to faecally contaminated water or food following a series of floods that washed away latrines into water sources in sub-counties of Nyakiyumbu, Bwera and Isango basing on our environment assessment report and interview with the cases and/or care takers.

Antimicrobial resistance of V. cholerae to the commonly used antibiotics was high.

Recommendation

Laboratory capacity to detect and monitor the rapidly emerging drug resistance among V. cholerae Isolates needs to be improved to effectively handle the dual challenge of treatment and prevention of Cholera. We also recommend proactive surveillance other than reactive surveillance to reduce the case fatality rate.

Generalizability

Our findings can be generalized to similar settings in Uganda and other developing countries.

OHCEA: One Health Central and East Africa; CFR: case fatality rate; WHO: World Health Organization; CLSI: Clinical and Laboratory Standards Institute; GWFS: Gravitational Water Flow Schemes; SDG: Sustainable Development Goals; GPS: Global Positioning System; IDRC: International Development Research Centre –Canada. Gen = Gentamycin, SXT = Trimethoprim/Sulfamethoxazole, Tet = Tetracycline, Nal = Nalidixic acid, Cip = Ciproflaxicin, Chl = Chloramphenicol, Amp = Ampicillin

Acknowledgements

We gratefully acknowledge our respondents both the cases and non-case who provided useful information for this work. Heartfelt thanks to Bwera hospital and Kagando hospital laboratories for supporting the isolation and susceptibility testing during the time of the cholera outbreak. We also thank Stallone Kisembo for the great work he did as a research assistant.

Funding

This work was supported by the International Development Research Centre (IDRC) - Canada; grant to One Health Central and Eastern Africa (OHCEA) and DELTAS Africa Initiative [grant# 107743/Z/15/Z]. The DELTAS Africa Initiative is an independent funding scheme of the African Academy of Sciences (AAS)’s Alliance for Accelerating Excellence in Science in Africa (AESA) and supported by the New Partnership for Africa’s Development Planning and Coordinating Agency (NEPAD Agency) with funding from the Wellcome Trust [grant #107743/Z/15/Z] and the UK government. The views expressed in this manuscript are those of the author(s) and not necessarily those of AAS, NEPAD Agency, Wellcome Trust or the UK government. The funding only covered data collection. This article did not receive sponsorship for publication.

Availability of data and materials

All data on which the conclusions of this manuscript are drawn are contained in the main manuscript and the tables herein.

Author Contributions

IJS participated in conception of the research idea, study design and drafting the first manuscript; CK participated in analysis and interpretation of the data, IBR conducted critical reviews and through his International Development Research Centre IDRC-Canada Ecohealth project partially funded the project and BBA conducted critical reviews and supervised the study. All authors have read and approved the final version of the manuscript.

Ethics approval and consent to participate

Consent for publication

Not applicable

Competing interest

The authors declare that they have no conflict of interest

Author’s details

¹Department of Medical Microbiology, College of Health Sciences, Makerere University, Kampala, Uganda. ²Department of Microbiology and Immunology, Faculty of Health Sciences, Busitema University, Mbale, Uganda. ³One Health Central and Eastern Africa (OHCEA) network, School of Public Health, Makerere University, Kampala, Uganda. ⁴Department of Biosecurity, Ecosystems and Veterinary Public Health, College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University Kampala, Uganda. ⁵One Health Division, College of Veterinary Medicine, University of Minnesota, St. Paul, MN, United States of America.

Shears P. Recent developments in cholera. Curr Opin Infect Dis. 2001;14(5):553-8.
Ali M, Lopez A, Ae You Y, Eun Kim Y, Sah B, Maskery B, et al. The global burden of cholera. Bull World Health Organ. 2012;90(3):209-18.
World Health. Cholera Organization. Cholera Cholera-Fact Sheet. 2014;107.
Mohammad Ali, Anna Lena Lopez, Young Ae You, Young Eun Kim, Binod Sah, Brian Maskery & John Clemens. The global burden of cholera. Bulletin of the World Health Organization. 2012;90(209):218.
Ivers LC. Strengthening the health system while investing in Haiti. Am J Public Health 101: 970–971. 2011;101:970-1.
Ben Taleb Z, Bahelah R, Fouad FM, Coutts A, Wilcox M, MaziakW. Syria: health in a country undergoing tragic transition. Int J Public Health 60 (Suppl 1): S63–S72. 2015;60:63-72.
Sule IB, Yahaya, M., Aisha, A. A., Zainab, A. D., Ummulkhulthum, B., & Nguku, P. (2017). Descriptive epidemiology of a cholera outbreak in Kaduna State, Northwest Nigeria, 2014. The Pan African medical journal. 2017.
Bwire G, Malimbo M, Maskery B, Kim YE, Mogasale V, Levin A. The burden of cholera in Uganda. PLoS Negl Trop Dis. 2013;7(12).
Benon Kwesiga, Gerald Pande, Alex Riolexus Ario, Nazarius Mbona Tumwesigye, Joseph K. B. Matovu and Bao-Ping Zhu. . A prolonged, community-wide cholera outbreak associated with drinking water contaminated by sewage in Kasese District, western Uganda. BMC Public Health. 2018;18(30).
Bwire G, Mwesawina M, Baluku Y, Kanyanda SSE, Orach CG. Cross-border cholera outbreaks in sub-Saharan Africa, the mystery behind the silent illness: what needs to be done? . PLoS One. 2016;11(6).
Uganda Ministry of Health. District Health Information System (DHIS2) Dashboard. 2018.
World Health,Organization. Assessing the Outbreak Response and Improving Preparedness. 2004.
Clinical and Lboratory Standareds Institute. M100-S25 Performance Standards for Antimicrobial Susceptibility Testing; 2014. 2014.
Cummings MJ, Wamala J, Eyura M, Malimbo M, Omeke ME, Mayer D, Lukwago L. A cholera outbreak among semi-nomadic pastoralists in northeastern Uganda: epidemiology and interventions Epidemiol Infect. 2012;140(8):1376-85.
World Health Organization. Uganda Hosts Traning on Disease outbreak for the African Region. 2017.
Afayo Robert. Muzamil Buga, John Bosco Alege., Pardon Akugizibwe, Christine Atuhairwe, and Ivan Mugisha Taremwa. Performance of Epidemic Preparedness and response Commitees to disease outbreaks in Arua District, West Nile Region. Journal of Environmental and Public Health. 2019;2019.
Ahebwa Amelia, Akol Walter, Achong Emmanuel, Mugerwa Timothy, Nakayenga Aminah, Omega Phillip, Rebecca Nekaka and Iramiot Jacob Stanley*. Awareness of Antimicrobial Resistance among Primary Health Care Workers in Buyende District, Rural Eastern Uganda. Microbiology Research Journal International. 2017;22(5):1-11.
Nicholas H. Gaffga RVT, and Eric D. Mintz. Cholera: A New Homeland in Africa? . The American Society of Tropical Medicine and Hygiene Am J Trop Med Hyg. 2007;77(4):705-13.
Curran KG, Wells, E., Crowe, S. J., Narra, R., Oremo, J., Boru, W., … Kioko, J. Systems, supplies, and staff: a mixed-methods study of health care workers' experiences and health facility preparedness during a large national cholera outbreak, Kenya 2015. BMC public health. 2018;18(1):723.
Pons W, Young I, Truong J, Jones-Bitton A, McEwen S, Pintar K,Papadopoulos A. A systematic review of waterborne disease outbreaks associated with small non-community drinking water Systems in Canada and the United States. PLoS One. 2015;10(10).
Taylor DL,ahawita KT, Cairncross S, Ensink JHJ. The impact of water, sanitation and hygiene interventions to control cholera: a systematic review. PLoS One. 2015;10(8).
Uthappa CK, Allam R, Nalini C, Gunti D, Udaragudi PR, Tadi GP, Murhekar MV. An outbreak of cholera in Medipally village, Andhra Pradesh. India Journal of Health, Population and Nutrition. 2015;33(1):1-5.
Uganda Bureau of Statistics. The National Population and Housing Census 2014- Main Report, Kampala, Uganda. 2016.
Uganda Ministry of Water and Environment. Water and Environment Performance Report 2017.
Barati HA, Golmhmmadi A, Momeni I, Mpradi G. A cholera outbreak investigation in Karaj district in 2008. Iran J Epidemiol. 2010;6(3):28-34.
Sedaghat M, Rahimi F, Talebi M, Pourshafie M. Serotyping, Antibiotic Susceptibility Pattern and Detection of hlyA Gene Among Cholera Patients in Iran. Jundishapur J Microbiol. 2012;6(1):20-3.

Download PDF

Journal Publication

published 29 Oct, 2019

Read the published version in BMC Public Health →

Editorial decision: Minor revision
15 Sep, 2019
Editor assigned by journal
13 Sep, 2019
Submission checks completed at journal
12 Sep, 2019
Editor invited by journal
12 Sep, 2019

You are reading this older preprint version

Read the latest preprint version →

Epidemiology and Antibiotic Susceptibility of Vibrio cholerae Associated with the 2017 Outbreak in Kasese district

Status:

Journal Publication

Version 2

Abstract

Figures

Background

Methods

Results

Discussion

Conclusion

Abbreviations

Declarations

References

Status:

Journal Publication

Version 2