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Background:
Systematic Review

Cholera Outbreaks in Low- and Middle-Income Countries in the Last Decade: A Systematic Review and Meta-Analysis

by
Anastasia A. Asantewaa
1,
Alex Odoom
1,
Godfred Owusu-Okyere
2 and
Eric S. Donkor
1,*
1
Department of Medical Microbiology, University of Ghana Medical School, Korle Bu, Accra P.O. Box KB 4236, Ghana
2
National Public Health & Reference Laboratory (NPHRL), Ghana Health Service-Korle Bu, Accra P.O. Box 300, Ghana
*
Author to whom correspondence should be addressed.
Microorganisms 2024, 12(12), 2504; https://doi.org/10.3390/microorganisms12122504
Submission received: 28 October 2024 / Revised: 14 November 2024 / Accepted: 19 November 2024 / Published: 4 December 2024
(This article belongs to the Special Issue Human Infectious Diseases)

Abstract

:
Cholera is linked to penury, making low- and middle-income countries (LMICs) particularly vulnerable to outbreaks. In this systematic review, we analyzed the drivers contributing to these outbreaks, focusing on the epidemiology of cholera in LMICs. This review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines and was registered in PROSPERO (ID: CRD42024591613). We searched PubMed, Scopus, Web of Science, and Google Scholar to include studies on cholera outbreaks that occurred in LMICs from 1 January 2014 to 21 September 2024. Studies on outbreaks outside LMICs and focusing on sporadic cases were excluded. The risk of bias among included studies was assessed using a modified Downes et al. appraisal tool. Thematic analysis was used to synthesize the qualitative data, and meta-analyses to estimate the pooled prevalence. From 1662 records, 95 studies met inclusion criteria, primarily documenting outbreaks in Africa (74%) and Asia (26%). Contaminated water was the main route of disease transmission. The pooled fatality prevalence was 1.3% (95% CI: 1.1–1.6), and the detection rate among suspected cases was 57.8% (95% CI: 49.2–66.4). Vibrio cholerae O1 was the dominant serogroup while Ogawa was the dominant serotype. All studies reporting biotypes indicated El Tor. Although the isolates were 100% susceptible to ofloxacin, levofloxacin, norfloxacin, cefuroxime, and doxycycline, they were also fully resistant to amikacin, sulfamethoxazole, trimethoprim, and furazolidone. The persistence of cholera outbreaks in destitute areas with limited access to clean water and sanitation emphasizes the need for socioeconomic improvements, infrastructure development, and ongoing surveillance to support timely responses and achieve long-term prevention.

1. Introduction

Cholera is an acute diarrheal disease caused by the toxigenic strains of Vibrio cholerae, particularly serogroups O1 and O139 [1]. With a short incubation period of two hours to five days, the disease can spread quickly through fecal contamination of water or food, resulting in explosive outbreaks that can overwhelm local health infrastructure [1]. While cholera can be asymptomatic or mild in some cases, severe infections can progress rapidly, with patients losing large volumes of fluid in a short period, making timely treatment critical to reducing mortality [2].
The recurrence of cholera is largely due to poor infrastructure and poverty, making LMICs especially vulnerable to repeated outbreaks [3]. Historically, the disease has been endemic in the Asian subcontinent and has triggered seven pandemics since 1817, with the most recent beginning in 1961 and still ongoing [4]. In recent years, cholera outbreaks have been reported in multiple countries. In 2021, 23 countries, mostly in the World Health Organisation (WHO) regions of Africa and the Eastern Mediterranean, experienced outbreaks. By November 2022, cholera cases had been documented in over 29 countries, with 16 nations suffering from prolonged outbreaks [2]. Yemen, for instance, saw over 2.5 million suspected cases and 4000 deaths between 2016 and 2022, marking one of the worst cholera outbreaks in modern history [5].
Although global efforts have been made to control cholera, the actual impact of the disease is likely much higher than reported figures suggest. The WHO estimates that cholera causes 3 to 5 million cases and 100,000 to 120,000 deaths each year, but many cases go unreported due to weak surveillance systems, resource constraints, and the stigma associated with the disease [6]. Additionally, cholera is often difficult to distinguish from other diarrheal diseases based solely on symptoms, complicating outbreak detection and management.
Many studies have documented cholera outbreaks in developing nations. However, a systematic examination of their causes and dynamics is lacking. Recent reviews [3,7] mainly focused on specific regions, such as India and Sub-Saharan Africa. To bridge this gap, we conducted a broader analysis of cholera outbreak characteristics and transmission dynamics across various LMICs. The results aim to provide a clear overview of cholera outbreaks and to act as a valuable resource for public health officials in controlling and managing the disease.

2. Materials and Methods

2.1. Search Strategy

This systematic review followed the PRISMA guidelines (Supplementary Table S1), [8] and was registered in PROSPERO (ID: CRD42024591613). We searched electronic databases including MEDLINE through PubMed, Scopus, Web of Science, and Google Scholar. The search covered studies published in English between 1 January 2014 and 21 September 2024. Keywords such as “cholera”, “outbreak”, and “cholera infection” were combined with specific names of LMICs to focus on relevant countries. The detailed search strategy is provided in Supplementary Table S2.
Search results were exported to Rayyan [9], where duplicates were identified and manually removed. Two reviewers screened the remaining studies by title and abstract, followed by full-text reviews to confirm eligibility. Any disparities regarding final study inclusion between the two reviewers were recognized and resolved through discussion and consensus. A third reviewer was available to mediate if consensus was not achieved; however, no intervention was needed.

2.2. Eligibility Criteria

2.2.1. Inclusion Criteria

Studies met the inclusion criteria if they:
  • Reported epidemiological data, including transmission routes and risk factors from a confirmed cholera outbreak in countries classified as LMICs by the World Bank [10];
  • Reported cholera outbreaks that occurred between 1 January 2014 and 21 September 2024;
  • Were original research articles with a focus on outbreak epidemiology. Study designs could be cross-sectional, cohort, case–control, or surveillance-based outbreak reports.

2.2.2. Exclusion Criteria

Studies were excluded if they:
  • Focused only on sporadic, endemic cholera cases rather than outbreak settings;
  • Only presented data as conference abstracts without full-text availability;
  • Were reviews, editorials, commentaries, and discussion pieces without primary epidemiological findings;
  • Presented epidemiological models or simulations rather than empirical outbreak investigation results;
  • Pertained to high-income countries, or cholera-endemic regions rather than outbreak events;
  • Addressed interventions, candidate vaccines, or treatment effectiveness rather than descriptive epidemiology.

2.3. Quality Assessment

The risk of bias in the included studies was evaluated by two reviewers using a modified Downes et al. appraisal checklist for cross-sectional studies (AXIS) [11]. The key factors evaluated were the clarity of the study objectives, description of the study design, and the presence of a clear definition of cholera. The appraisal tool also examined sampling methods, reporting of outcomes such as risk factors and case fatality rates, and the rigor of data collection and statistical analysis. Additionally, the use of diagnostic methods such as culture or PCR for cholera confirmation, along with discussions of limitations and confounders, was considered. Based on these criteria, each study was rated as having a low, moderate, or high risk of bias.

2.4. Data Extraction and Synthesis

Data, including geographic location, region, study design, and timeframe of the cholera outbreak, were extracted using an Excel spreadsheet (Version 2410). Variables like the number of cases, transmission routes, and case fatality ratios (CFR) were also captured, as well as any identified risk factors such as water contamination and poor sanitation. Additionally, details on the V. cholerae serogroup, serotypes, and biotypes were documented, and antibiotic resistance data were included where applicable. The results were thematically synthesized and presented in textual narrative formats, tables, and figures. A random-effects meta-analysis with 95% confidence intervals was conducted to estimate the pooled prevalence of laboratory-confirmed cases and overall disease fatality. Heterogeneity was statistically assessed using the I2 metric and Chi-squared test. Subgroup analyses explored potential sources of heterogeneity by region. Publication bias was statistically assessed using Egger’s tests, and graphically using funnel plots.

3. Results

3.1. Search Results

In total, 1662 records were identified through searches in PubMed (n = 193), Scopus (n = 768), Web of Science (n = 301), and the first 400 results from Google Scholar. After removing 589 duplicates, 1073 records were screened. Of these, 847 were excluded due to irrelevance based on the title and abstract, language limitations, and review articles. This left 224 records for eligibility assessment, from which 128 were excluded for reasons such as not fitting the scope, not being outbreak studies, occurring outside the decade under review, non-LMIC settings, being duplicates, or inaccessible full texts. Ultimately, 95 studies were included in the final review [12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106] (Figure 1).

3.2. Risk of Bias

Of the 95 studies assessed, 44 (46.3%) were classified as having a low risk of bias, 41 (43.2%) were rated as moderate risk, and 10 (10.5%) were scored as high risk (Table S3).

3.3. Study Characteristics

The 95 included studies reporting on cholera outbreaks across 24 countries were all recognized as LMICs by the World Bank [10]. The studies were primarily from Africa (n = 70; 74.0%) and Asia (n = 25; 26.0%), with most of them from India and Uganda, each with 10 studies (Figure 2).
Cholera outbreaks documented in the included studies spanned from 2014 to 2024. While some studies reported protracted outbreaks covering multiple years, none reported an outbreak in 2020 (Figure 3, Table A1). The highest number of outbreaks began in 2017 (Figure 3), with several outbreaks continuing into subsequent years. The peak number of suspected cholera cases was recorded between 2016 and 2018, totaling over 2.3 million cases (Table A1).
More than 2.8 million suspected cases of cholera were reported. Yemen accounted for 80% of these cases, with 2.3 million suspected cases, whereas Malaysia reported the fewest cases, with only 78 cases. Other countries with substantial case numbers included Ghana, Nigeria, Malawi, and Tanzania, each reporting over 50,000 cases. Meanwhile, Pakistan, Algeria, the Central African Republic, and Mozambique reported fewer than 1000 cases (Figure 4, Table A1).

3.4. Routes of Cholera Transmission

Water contamination was the primary source of disease transmission throughout the decade (Figure 5) and across multiple countries (Figure 6). All outbreaks that began in 2021 were attributed to contaminated water sources. Moreover, it was reported as the sole transmission route for cholera outbreaks reported in Tanzania. Overcrowding and person-to-person contact were also noted as significant drivers of outbreaks in Kenya and Sudan, while open defecation played a role in Ghana, India, Uganda, and Ethiopia. Humanitarian crises and natural disasters such as protracted wars, floods, and cyclones also triggered outbreaks in Yemen, Iraq, Nigeria, Mozambique, Uganda, and Zambia, creating ideal conditions for cholera to spread across these regions. The other drivers were food contamination, poor hygiene and sanitation, and a lack of resources.

3.5. Pooled Prevalence of Cholera-Induced Fatality

Based on a random-effect meta-analysis of 69 studies, the pooled fatality prevalence during outbreaks was 1.3% (95% Cl: 1.1–1.6). In terms of regional variation, Africa had a higher fatality prevalence (1.5%) compared to Asia (0.3%) (Figure 7). This variance suggests differing levels of outbreak impact or healthcare response effectiveness between the regions.

3.6. Laboratory-Confirmed Cholera Cases During Outbreaks

The pooled detection rate of laboratory-confirmed cholera among suspected cases was 57.8% (95% Cl: 49.2–66.4) based on a random-effects meta-analysis of 49 studies. Africa had a higher rate of laboratory-confirmed cholera 62.9% compared to Asia (45.6%) (Figure 8).

3.7. V. cholerae Strain Classification

V. cholerae O1 was the predominant serogroup, accounting for 94.5% of the outbreaks, followed by V. cholerae O139 at 3.64% and non-O1/O139 at 1.81%. All identified isolates were classified under the El Tor biotype, with no instances of the classical biotype. Regarding serotypes, Ogawa was the most common (76.1%), Inaba comprised 15.2%, and a combination of both Ogawa and Inaba appeared in 0.065% of the reported outbreaks (Table A2).

3.8. Antimicrobial Resistance Patterns

Data from 14 of 95 studies provided antimicrobial susceptibility testing (AST) results for 799 V. cholerae isolates against a range of antibiotics. Notably, several antibiotics exhibited high efficacy, with ofloxacin, levofloxacin, norfloxacin, cefuroxime, and doxycycline having susceptibility rates of at or near 100%. Conversely, ampicillin, cotrimoxazole, sulfamethoxazole, trimethoprim, amikacin, and furazolidone displayed extremely high resistance rates, with over 80% of isolates resistant, indicating their limited utility in treating these cholera strains (Figure 9).

4. Discussion

Since the seventh pandemic emerged in South Asia in 1961, cholera has not only continuously affected the region but also become endemic in several countries across Africa, Asia, and South America. In this review, while our focus was on low- and middle-income countries globally, we observed that the reported outbreaks in the included studies were in Africa (74.0%) and Asia (26.0%). Notably, Yemen recorded the highest number of suspected cases, with over 2.3 million cases reported during a protracted outbreak from 2016 to 2022 [25,35,93,106]. This outbreak, considered the worst cholera epidemic of modern times [107], was largely fuelled by the country’s ongoing civil war between pro-government forces and the Houthi armed movement, which severely weakened already fragile sanitation and healthcare systems [108].
Similarly, in Nigeria and the Democratic Republic of the Congo, conflict has been associated with increased rates of cholera outbreaks by 3.6 and 2.6 times, respectively [109]. Poor urban settlements, overcrowded conditions, and lack of access to water, sanitation, and hygiene make these areas particularly vulnerable to outbreaks during times of conflict [110]. In Syria, the destruction of water treatment facilities during an ongoing conflict left nearly half of the population relying on unsafe water sources to complement their daily water needs [16,111].
Other humanitarian crises caused by natural disasters such as floods, heavy rainfall, and cyclones were also identified as drivers of cholera outbreaks in this review [18,24,27,33,63]. For example, Cyclone Kenneth, which struck northern Mozambique in April 2019, severely damaged water and sanitation infrastructure, leading to a cholera outbreak [26]. Similarly, in Malawi, Cyclone Ana (January 2022) and Cyclone Gombe (March 2022) caused torrential rains and flooding, which overwhelmed water systems and overcrowded settlements, creating ideal conditions for cholera transmission [18,112]. Moreover, torrential rains and floods in early 2022 displaced many people in southern Malawi and left them without access to safe drinking water, further increasing the risk of cholera [18].
Across many cholera-prone areas, water contamination was identified as the primary transmission route, particularly in rural areas where rivers, hand-dug wells, deep wells, and springs serve as water sources [21,43,80,87,95]. These water sources are often poorly protected, making them unsafe for household use. Eyu et al. observed that community members used the river as a source of drinking water, as well as for washing clothes, kitchen utensils, and bathing, despite the river’s turbid and unprotected condition [43]. These unimproved water sources increase the odds of cholera infection by threefold [113]. Similarly, a significant link was found between drinking water from the Zamani River, a source of drinking water, and a cholera outbreak in a rural community in Nigeria [31]. In Ghana, Issahaku et al. found that pipelines passing through open drainage systems are highly susceptible to contamination, especially when damaged [55]. Furthermore, investigations during outbreaks have frequently revealed water sources contaminated with fecal matter, a major driver of Vibrio cholerae infections [55]. For instance, in North Karnataka, India, water samples were found to be heavily contaminated with fecal coliforms, indicating poor sewage disposal and unclean water sources [114]. Additionally, residents in Sembule Village, Uganda, were found to empty fecal waste into a drainage channel connected to a well (used as a drinking water source), particularly during rainfall when the waste was more likely to be washed away [42]. In another study in India, fecal matter was discovered in pond water that locals used for drinking and preparing fermented rice (Panta Bhat) [115]. Strikingly, the villagers believed that the fermented rice tasted better when prepared with pond water [115]. This indicates a lack of awareness of the health risks associated with contaminated water.
In countries such as India, Ghana, and Uganda, where open defecation is a persistent issue, it has been identified as a significant driver of cholera outbreaks [36,54,88,90]. Rainwater runoff frequently carries human waste into nearby rivers and water sources, worsening contamination and increasing the risk of V. cholerae infection [90]. According to studies by Iramiot et al. and Eyu et al., most latrines in affected areas are unimproved, which likely encourages widespread open defecation [43,54]. In Uganda, the National Housing and Population Census reported that while only 10% of the rural population lacks access to pit latrines, approximately 58% of the existing pit latrines are unimproved, contributing to the ongoing cholera risk [54].
While Challa et al. found that individuals who practiced water purification methods had a lower chance of contracting cholera [28], Davis et al. observed that despite extensive water chlorination efforts, cholera outbreaks were prolonged by the continued consumption of contaminated food in Ethiopia [32]. In many settings in Kenya, Malaysia, Ethiopia, Sudan, Bangladesh, and Syria, food contamination is a major cause of cholera outbreaks [16,41,47,50,57,79,88].
Research has consistently shown that certain foods, such as seafood, uncooked vegetables, and cold leftover rice, are vehicles for cholera outbreaks, as they may harbor V. cholerae strains [32,116]. These bacteria can thrive in improperly handled or stored food, making them a significant source of infection [32]. However, previous studies have indicated that heating food thoroughly can effectively kill V. cholerae, greatly reducing the risk of transmission [32,117]. In Jijiga, Ethiopia, a spike in cholera cases coincided with Ramadan, a time when there was an increase in street food vendors selling Iftar meals [32]. Anecdotal evidence suggests that many of these vendors were unlicensed and may not have followed proper food safety protocols, contributing to the outbreak. Similarly, in Ghana, where unlicensed street food vendors are prevalent [55], it was found that eating street-vended food was associated with a sixfold increase in the odds of contracting cholera [118].
Additionally, studies have consistently shown that attending social events where food is served, particularly in informal or outdoor settings, significantly increases the risk of cholera transmission [32,55]. In Dadaab refugee camp in Kenya, Golicha et al. documented that the worst cholera outbreak since 1992 was linked to its proximity to bustling food markets where individuals from regions affected by cholera frequently gathered [50]. Some included studies in this review also reported that person-to-person contact, and overcrowding exacerbated the outbreaks [31,64,80]. A systematic review in India shed light on this mode of transmission and revealed that V. cholerae can be transmitted by coming into contact with cholera patients or asymptomatic carriers [3]. It has been explained that transmission often occurs through fomites, food, or water within households [3]. Without proper hygiene practices, such as handwashing, people who come into contact with these contaminated surfaces unknowingly spread the bacteria, further perpetuating the cholera outbreak via the fecal–oral route [3,119].
To control the spread of the disease during outbreaks, the Global Task Force on Cholera Control (GTFCC) advocates for the swift distribution of emergency WASH (water, sanitation, and hygiene) resources, such as water purification devices and emergency latrines, along with deployment of rapid response teams equipped with the case-area targeted intervention (CATI) strategy [120,121,122]. CATI targets the early identification of cholera clusters to enable a focused response within a high-risk radius around affected households, aiming to quickly reduce transmission and contain the outbreak [89,121].
In this review, we found that the overall detection rate of laboratory-confirmed cholera among suspected cases was 57.8% (95% CI: 49.2–66.4). Interestingly, Africa had a higher confirmation rate (62.9%) than Asia (45.6%), although the number of suspected cases was higher in Asia. This difference can be attributed to the greater number of outbreaks documented in Africa in this review. Cholera outbreaks are typically defined by the presence of at least one confirmed case of cholera along with evidence of local transmission [123]. Once an outbreak is declared, it is no longer necessary to confirm every suspected case; hence, a clinical case definition is considered sufficient for tracking epidemiological trends. However, for an outbreak to be officially declared, V. cholerae O1 or O139 must first be confirmed either by culture or PCR [123].
Among the more than 200 known serogroups of V. cholerae, only O1 and O139 have been consistently linked to cholera epidemics [4]. In this study, V. cholerae O1 emerged as the predominant serogroup. This dominance is largely due to the El Tor biotype, which can thrive in diverse environmental settings and cause asymptomatic infections, allowing cholera outbreaks to persist and spread over time [4,124]. The current cholera pandemic has been driven primarily by the El Tor biotype, which has effectively displaced the classical biotype, now considered extinct since its last recorded occurrence in the 1980s [125]. As expected, all included studies that reported the biotype confirmed the presence of El Tor.
The O1 strains are classified into three serotypes: Ogawa, Inaba, and Hikojima, which differ according to the methylation of the terminal perosamine in their oligosaccharide structures [124]. Ogawa, which is methylated, was responsible for 76.1% of cholera outbreaks, whereas Inaba, which is an unmethylated form, accounted for 15.2%. Ogawa and Inaba serotypes often co-circulate during epidemics and can interconvert [4,126]. This was observed in some studies that reported outbreaks (0.065%) with both serotypes existing [17,105]. This antigenic switching enables V. cholerae to evade immune detection and sustain transmission [4].
V. cholerae O139, which appeared in the early 1990s, has largely been confined to South and Southeast Asia [4,124]. Nevertheless, we observed its presence in outbreaks in Kenya and Uganda, indicating possible geographic expansion. Additionally, we observed one case of non-O1, non-O139 Vibrio cholerae (NOVC) associated with an outbreak [14]. Although NOVC strains do not produce cholera toxins and do not cause cholera, studies suggest that they account for between 1% and 3.4% of acute diarrheal cases worldwide [127,128].
Eliminating cholera has been a global priority, and the GTFCC introduced the “Ending Cholera: The Global Roadmap to 2030” strategy [129]. This framework envisions a world in which cholera no longer poses a public health threat, aiming to reduce cholera deaths by 90% and eliminate the disease in 20 countries [129]. We observed the pooled fatality prevalence during cholera outbreaks to be 1.3% and 1.3% (95% Cl: 1.1–1.6). This exceeds the minimum acceptable standard of less than 1% and reflects shortcomings in healthcare access and case management during outbreaks. Specifically, Africa had a significantly higher CFR (1.5%) than Asia (0.3%). CFR is a key indicator of healthcare quality during cholera outbreaks, with lower rates suggesting better access to treatment and timely interventions [130]. In Africa, limited resources, underfunded healthcare systems, and logistical challenges in providing timely treatment likely contribute to higher mortality [131,132].
Cholera treatment focuses on several key agents, including oral rehydration therapy (ORT), intravenous fluid therapy, antibiotics, and, in some cases, oral cholera vaccines (OCVs) [133]. The primary goal of this approach is to rehydrate patients and prevent dehydration, which is the leading cause of death in cholera cases [134,135]. The most widely recommended treatment is ORT, which involves administering a solution of salts and glucose to replace lost fluids and electrolytes [136,137]. In severe cases of extreme dehydration, intravenous fluids may be required to restore hydration rapidly [138].
Antibiotic therapy is another important treatment, particularly for patients with severe cholera. Although the World Health Organisation (WHO) recommends using antibiotics only for severe dehydration, the International Centre for Diarrhoeal Disease Research (ICDDR, B) recommends broader use, including for patients with moderate dehydration who continue to pass large amounts of diarrhea despite rehydration therapy [139]. Antibiotic therapy not only reduces illness duration but also limits transmission. Effective antibiotics can reduce the period during which patients shed V. cholerae from five or more days to just one or two days [139,140]. In a systematic review of antimicrobial drugs against V. cholerae, antimicrobial therapy was found to shorten the duration of diarrhea by about 1.5 days, reduce stool volume by 50%, and decrease the need for rehydration fluids by 40% [140]. The use of antibiotics not only accelerates recovery but also reduces the volume of rehydration fluids required and shortens the duration of hospitalization [133]. Studies have demonstrated the effectiveness of antibiotics like doxycycline and azithromycin, which can dramatically reduce diarrhea within 24 h, allowing patients to recover faster and leave treatment centers earlier [139,141].
One drawback to antibiotic therapy is that the V. cholerae O1 and O139 strains have developed resistance to most of the antibiotics that are used [142]. In this review, while most of the isolates showed susceptibility to antibiotics like ofloxacin, levofloxacin, norfloxacin, cefuroxime, doxycycline, and azithromycin, most of the isolates were resistant to traditional first-line antibiotics like ampicillin, cotrimoxazole, and amikacin. Most isolates also showed resistance to sulfamethoxazole, trimethoprim, furazolidone, and nalidixic acid.
To reduce the antimicrobial resistance of V. cholerae, the GTFCC provides specific guidance for selecting antibiotics during cholera outbreaks [123]. According to their recommendations, antibiotics should be selectively targeted to patients most likely to benefit clinically. The selection of antibiotics must be guided by current evidence on the sensitivity of circulating cholera strains, with regular monitoring for evolving resistance during outbreaks where feasible. Single-dose regimens are highly preferred over multi-dose treatments to facilitate easier implementation, particularly during large-scale outbreaks, and factors such as availability, cost, and ease of use are also important considerations when selecting an antibiotic [123]. The WHO advocates for the use of OCVs, particularly in endemic areas and during outbreaks [133,143]. When combined with ORT and antibiotics, OCVs provide temporary immunity and help reduce transmission risks [144].
We acknowledge some limitations in this review. The conclusions were primarily derived from peer-reviewed articles on cholera outbreaks, which may not fully reflect the actual incidence of outbreaks because of heterogeneity in reporting standards across regions. Moreover, we were unable to assess seasonal trends during the outbreaks, which could have enhanced our understanding of the epidemiology of the disease.

5. Conclusions

Cholera persists in impoverished areas, particularly in regions where crises weaken access to clean water and sanitation. Though treatments like doxycycline and azithromycin help manage such cases, the long-term solution lies in prevention. We advocate for the targeted deployment of cholera vaccines and the provision of safe drinking water through the chlorination of water sources and regular disinfection of tube wells. Moreover, public education on hygiene and upgrading of sewage systems is key to controlling outbreaks. Continuous surveillance will also ensure prompt action during future outbreaks.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/microorganisms12122504/s1, Table S1: PRISMA Checklist [145]; Table S2: Search Strategy; Table S3: Risk of Bias Assessment of Included Studies; Figure S1: Funnel Plot of Studies on Fatality Cases.

Author Contributions

Conceptualization, E.S.D.; methodology, A.A.A. and A.O.; formal analysis, A.A.A. and A.O.; data curation, A.A.A. and A.O.; writing—original draft preparation, A.A.A.; writing—review and editing, A.O., G.O.-O. and E.S.D.; visualization, A.A.A. and A.O.; supervision, E.S.D.; project administration, E.S.D.; funding acquisition, E.S.D. All authors have read and agreed to the published version of the manuscript.

Funding

This review paper was supported by the Fogarty International Center of the National Institutes of Health through the Research and Capacity Building in Antimicrobial Resistance in West Africa (RECABAW) Training Programme hosted at the Department of Medical Microbiology, University of Ghana Medical School (Award Number: D43TW012487). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Table A1. Study characteristics of included studies.
Table A1. Study characteristics of included studies.
StudyCountryRegionLocationStudy Design/TypeOutbreak OccurrencePopulation at RiskNo. of CasesCFR (No. of Deaths)
Abou et al., 2024 [12]LebanonAfrica_Descriptive 6 October 2022 to June 2023_800711% (23 deaths)
Abu Bashar et al., 2022 [13]IndiaAsiaNakhrauli Village, Ambala DistrictDescriptive 20 July 201813001182 deaths
Amadu et al., 2021 [14]NigeriaAfricaIlorin MetropolisRetrospective descriptive January to September 2017_5138136 deaths
Alzain et al., 2021 [15]SudanAfricaNorthern StateDescriptive February and September 2017675,4819571.9%
Arnauot et al., 2024 [16]SyriaAsia_Prospective observational cohort study 20 September to 20 October 2022171210610.2%
Awuor et al., 2020 [17]KenyaAfricaKisumu CountyDescriptive (Cross-sectional)January to December 2017_ _
Bagcchi et al., 2022 [18]MalawiAfrica_Descriptive (Outbreak report)3 March 2022_785.1% (4 deaths)
Benamrouche et al., 2022 [19]AlgeriaAfricaBouira, Blida, Algiers, Tipaza, Aïn Defla, Médéa and OranDescriptive August 14 to 27 September 2018_291_
Berhe et al., 2024 [20]EthiopiaAfricaGuraghe ZoneDescriptive August 7 to 30 October 2023234,1612242.6% (6 deaths)
Bitew et al., 2024 [21]EthiopiaAfricaOromia National Regional State, Amhara National Regional State, Addis Ababa City Descriptive (Cross-sectional)26 September to 31 October 2023_ _
Bompangue et al., 2020 [22]Democratic Republic of the CongoAfricaKinshasaDescriptive analysis (Cross-sectional)January 2017 to November 201812 million1712_
Breurec et al., 2021 [23]Central African RepublicAfrica_Descriptive July to Dec 2016_26520 deaths
Bwire et al., 2023 [24]UgandaAfricaBududa DistrictCross-sectionalJune to August 2019259,800671.5% (1 death)
Camacho et al., 2018 [25]YemenAsia_Descriptive28 September 2016 to 12 March 201829,932,9711,103,6830.22 (2385)
Cambaza et al., 2019 [26]MozambiqueAfricaCabo Delgado ProvinceDescriptive2 May 2019_1490
Chaguza et al., 2024 [27]MalawiAfrica_Descriptive 2022 to 2023_59,1563% (1759 deaths)
Challa et al., 2022 [28]UgandaAfricaErer DistrictDescriptive (Case–control)4 September to 1 November 201969,129110_
Chibwe et al., 2020 [29]MalawiAfricaNsanje and Chikwawa DistrictsDescriptiveMarch 2018_2524 deaths
Chirambo et al., 2016 [30]ZambiaAfricaChibombo DistrictDescriptive (Cross-sectional)9 February to 20 March 2016568823_
Dan-Nwafor et al., 2019 [31]NigeriaAfricaGomali, Kwali Local Government AreaDescriptive (Case–control)October–November 20141000_1.3 (6 deaths)
Davis et al., 2023 [32]EthiopiaAfricaJijigaDescriptive (Case–control)1 January to 10 July_1000_
Denue et al., 2018 [33]NigeriaAfricaBorno StateDescriptive 14 August 20171,489,63858890.87% (43 deaths)
Dinede et al., 2020 [34]EthiopiaAfricaAddis AbabaDescriptive (Case–control)7 September 2017 to 1 October 2017_250
Dureab et al., 2019 [35]YemenAsiaAdenDescriptive (Case–control)1 January to 31 March 2018___
Dutta et al., 2021 [36]IndiaAsia Ghughri Descriptive (Case–control)18 August 2016_6282% (14 deaths)
Eibach et al., 2016 [37]GhanaAfrica_Descriptive 20 May 2014_20,1200.8% (165 deaths)
Elfaki et al., 2023 [38]SudanAfricaBlue Nile StateDescriptive20181250210
Elimian et al., 2020 [39]NigeriaAfrica_Descriptive (Cross-sectional)1 January–Nov ember 19_41,3941.97% (2 deaths)
Emmanuel et al., 2019 [40]ZimbabweAfricaHarare CityDescriptive (Cross-sectional)5–25 September 2018_35640.9% (31 deaths)
Endris et al., 2019 [41]EthiopiaAfricaAddis AbabaDescriptive8 June to 31 October 20163,435,02880830.18% (15 deaths)
Eurien et al., 2021 [42]UgandaAfricaKampala City, Sembule VillageDescriptive (Case–control)28 December 2018 to 11 February 20194700506% (4 deaths)
Eyu et al., 2022 [43]UgandaAfricaNebbi DistrictDescriptive (Case–control)10 February 2017409,0002221.35% (3 deaths)
Fagbamila et al., 2023 [44]NigeriaAfricaBauchi StateDescriptive (Case–control)28 February to 31 March 20194,653,06697250.3% (28 deaths)
Faruque et al., 2021 [45]BangladeshAsia-Descriptive (Cross-sectional)September–December 2019_368_
Feglo et al., 2018 [46]GhanaAfrica-Descriptive2014_28,975243 deaths
George et al., 2018 [47]BangladeshAsiaMathbaria and BakerganjDescriptive (Cross-sectional)April 2015 to June 2016_1081_
Gopalkrishna et al., 2019 [48]IndiaAsiaAurangabadDescriptive (Case–control)10 November 201716,0007447_
Goswami et al., 2019 [49]IndiaAsiaWardhaDescriptive (Cross-sectional)July104280
Golicha et al., 2018 [50]KenyaAfricaDadaab Refugee CampCase–control18 November 2015–6 June 2016340,00017970.79% (14 deaths)
Githuku et al., 2016 [51]KenyaAfricaHoma Bay CountyDescriptive January to April 2015_11,0331.6% (178 deaths)
Grandesso et al., 2019 [52]MalawiAfricaLake ChilwaDescriptive (Case–control)March to June 2016_2360 deaths
Helou et al., 2023 [53]LebanonAfrica_Outbreak reportOctober to December 2022_510523 deaths
Iramiot et al., 2019 [54]UgandaAfricaKasese DistrictDescriptive (Cross-sectional)September 2017 to January 2018757,2692221.4 (3 deaths)
Issahaku et al., 2020 [55]GhanaAfricaCentral RegionDescriptive (Case–control)12 October 2016 to 4 January 2017160,8497040
Jain et al., 2021 [56]IndiaAsiaShahpur Huts, Panchkula District, Haryana StateDescriptive (Case–control)1–28 September 2019_1961% (2 deaths)
Jikal et al., 2019 [57]MalaysiaAsiaSabahDescriptive (Case–control)20 December 2014_78_
Jones et al., 2020 [58]South SudanAfrica_Descriptive 2014–201711,65428,645622 deaths
Junejo et al., 2023 [59]PakistanAsiaKarachiDescriptive 2022_129_
Kanu et al., 2018 [60]NigeriaAfricaAndoni, Rivers StateDescriptive (Case–control)January 2015211,00910341.84% (19 deaths)
Kapata et al., 2018 [61]ZambiaAfrica_DescriptiveOctober 2017–February 2018_39382.1% (82 deaths)
Kaponda et al., 2019 [62]MalawiAfricaKaronga DistrictDescriptive (Cross-sectional)November 2017 and March 2018365,0003471.2% (4 deaths)
Kateule et al., 2024 [63]ZambiaAfricaLusaka DistrictDescriptive18 October 2023–February 20242,248,14013,1222.8% (368 deaths)
Kisera et al., 2020 [64]KenyaAfricaKakuma and KalobeyeiDescriptive (Cross-sectional)May 2017–2018185,543 0.8% (1 death)
Kumar et al., 2022 [65]IndiaAsiaRahude Village, Nashik, MaharashtraDescriptive 8–13 July 20188501951.03% (2 deaths)
Kigen et al., 2020 [66]KenyaAfricaNairobi CountyDescriptive (Case–control)December 2014–June 20154,232,08742181.9% (79 deaths)
Kwesiga et al., 2017 [67]UgandaAfricaKasese DistrictDescriptive (Case–control)May 2015702,0291832 deaths
Madulla et al., 2023 [68]TanzaniaAfricaMwanza CityDescriptive (Cross-sectional)August 2015–April 2016706,4538520.80 (7 deaths)
Matapo et al., 2016 [69]ZambiaAfricaLusakaDescriptive (Case–control)February and May 201629,8434410.9 (4 deaths)
Mashe et al., 2020 [70]ZimbabweAfrica_Descriptive 4 September 2018 to 12 March 20196,148,24310,7300.6% (69 deaths)
Matimba et al., 2022 [71]TanzaniaAfrica-Descriptive (Cross-sectional)August 2015 to December 2017_28,0891.6% (452 deaths)
Mbala-Kingebeni et al., 2021 [72]Democratic Republic of the CongoAsiaKinshasaDescriptive (Case–control)November 2017 to March 2018___
McCrickard et al., 2017 [73]TanzaniaAfricaDar es SalaamDescriptive 15 August 2015 to 31 October 2015_33711.1% (36 deaths)
Monje et al., 2020 [74]UgandaAfricaKyangwali Refugee Settlement, Hoima DistrictDescriptive (Case–control)1 February to 9 May 2019668,90021222.1% (44 deaths)
Mukhopadhyay et al., 2019 [75]IndiaAsiaKolkata MetropolisDescriptive (Cross-sectional)August 2015_3003_
Mutale et al., 2020 [76]ZambiaAfricaLusakaDescriptive (Case–control)6 October 201748536613% (20 deaths)
Mwaba et al., 2018 [77]ZambiaAfricaLusakaDescriptive 4 February to 15 June 20162.3 million251_
Mwape et al., 2020 [78]ZambiaAfricaLusakaDescriptiveFebruary to June 2016_>100022 deaths
Mwenda et al., 2017 [79]KenyaAfricaHotel in NairobiDescriptive20 June 2017 456456_
Nanzaluka et al., 2020 [80]ZambiaAfricaLusakaDescriptive (Case–control)6 October 2017_14622.6% (38 deaths)
Neamin et al., 2020 [81]EthiopiaAfrica_Descriptive2015 to 20179,653,371636,1540.7% (246 deaths)
Ngere et al., 2024 [82]KenyaAfricaNairobi CountyDescriptive (Cross-sectional)20174,697,27427371.5% (35 deaths)
Ngere et al., 2022 [83]KenyaAfrica_Retrospective cohort study31 August 2017 to 6 September 20175261390.7% (1 death)
Ngwa et al., 2020 [84]NigeriaAfricaBorno StateDescriptive (Cross-sectional)August 2017_53401.14% (61 deaths)
Noora et al., 2017 [85]GhanaAfricaBrong Ahafo RegionDescriptive July to December 20142.6 million10350.024
Nsubuga et al., 2019 [86]SudanAfricaTonj East and Tonj NorthDescriptive 1 May to 15 October 2017412,96914513.0% (44 deaths)
Oguttu et al., 2017 [87]UgandaAfricaKaiso Village, Hoima DistrictDescriptive (Case–control)1 October to 2 November 201590001222 deaths
Ohene-Adjei et al., 2017 [88]GhanaAfrica_Descriptive (Cross-sectional)June 2014 to January 20154,530,90520,1990.6% (121 deaths)
Okeeffe et al., 2024 [89]NigeriaAfricaBorno, Adamawa, and Yobe StatesProspective observational cohort study September to December 20211,538,000111,0623.2% (3604 deaths)
Okello et al., 2019 [90]UgandaAfricaBulambuli DistrictDescriptive (Case–control)1 March 2016_ _
Pande et al., 2018 [91]UgandaAfricaKasese DistrictDescriptive (Case–control)20 June 20151232461_
Patel et al., 2022 [92]IndiaAsiaNadiad CityDescriptive25 June 20212,540,0371580.63% (1 death)
Qaserah et al., 2021 [93]YemenAsiaAl HudaydahDescriptive (Case–control)December 1 2017 to January 10 2018400,00088,741244 deaths
Roobthaisong et al., 2017 [94]MyanmarAsiaMandalayDescriptive 2015_1617_
Roy et al., 2024 [95]IndiaAsiaDangapara Village, West BengalDescriptive 27 March 2021 to 8 April 2021330950
Sabir et al., 2023 [96]IraqAsiaSulaymaniyah ProvinceDescriptive June–July 2022_4754_
Shah et al., 2022 [97]IndiaAsiaGujaratDescriptive 2015 to 2016_4371.1% (1 death)
Sinyange et al., 2018 [98]ZambiaAfricaLusakaDescriptive October 2017–May 2018_54141.8 (98 deaths)
Sule et al., 2017 [99]NigeriaAfricaKaduna StateDescriptive 20147.685 million14683.68 (54 deaths)
Ujjiga et al., 2015 [101]South SudanAfrica_Descriptive (Case–control)23 April 2014_22602.0% (43 deaths)
Wang et al., 2016 [102]TanzaniaAfrica_Descriptive August 2015 to June 2016_21,750341 deaths
Winstead et al., 2020 [103]ZimbabweAfricaHarare ProvinceDescriptive September 2018–March 2019_10,7300.64% (69)
Zahid et al., 2022 [104]PakistanAsiaKarachiObservational March to May 2022___
Zgheir et al., 2019 [105]IraqAsia_Descriptive August 2017_13670.6% (30 deaths)
Zhao et al., 2019 [106]YemenAsia_Descriptive May 2017 to 2018_111,35782310 deaths
Table A2. Causes of cholera outbreaks.
Table A2. Causes of cholera outbreaks.
StudyRisk Factors Assessed Transmission Route/Suspected ExposureSerogroupSerotype/BiotypeNumber ExaminedNumber Infected
Abou et al., 2024 [12]--V. cholerae O1Ogawa/ El Tor-671
Abu Bashar et al., 2022 [13]Water source (filtration method or purifier, storage method), history of travel, mass gathering attendanceWaterborneV. cholerae O1Ogawa/ El Tor31
Amadu et al., 2021 [14]--V. cholerae O1Inaba and non-O1/O13910242
Al Zain et al., 2021 [15]-Travel----
Arnauot et al., 2024 [16]Water source (well water, swimming pool), foodWaterborne, foodborne-----
Awuor et al., 2020 [17]--V. cholerae O1Ogawa and Inaba/El Tor119101
Bagcchi et al., 2022 [18]--V. cholerae O1Inaba--
Benamrouche et al., 2022 [19]--V. cholerae O1Ogawa/ El Tor29191
Berhe et al., 2024 [20]-Poor hygiene and sanitation- --
Bitew et al., 2024 [21]Water source, outbreak season, toilet use frequencyWaterborneV. cholerae O1Ogawa--
Bompangue et al., 2020 [22]-Waterborne, poor hygiene and sanitation----
Breurec et al., 2021 [23]-Waterborne, poor hygiene and sanitation, overcrowding, lack of latrinesV. cholerae O1Inaba/ El Tor--
Chaguza et al., 2024 [27]-Cyclone GombeV. cholerae O1Ogawa/ El Tor4442
Challa et al., 2022 [28]Water source, eating habits, hygiene and sanitationPoor hygiene and sanitation----
Chibwe et al., 2020 [29]-FloodV. cholerae O1Ogawa8057
Chirambo et al., 2016 [30]-Waterborne, poor sanitation, inadequate sanitary facilities --188
Dan-Nwafor et al., 2019 [31]Water source, hygiene and sanitation, >5 persons per household, No formal education, Lack of rack for drying platesWaterborne, poor personal hygiene, overcrowding--44
Davis et al., 2023 [32]Water source, eating habits, hygiene and sanitationWaterborne----
Denue et al., 2018 [33]-Heavy rain, floodingV. cholerae O1Ogawa--
Dinede et al., 2020 [34]Water source, eating habits, hygie and sanitationWaterborne, foodborne- 7-
Dureab et al., 2019 [35]Travel history, water source, eating habits, hygiene and sanitationFoodborne, contact----
Dutta et al., 2021 [36]Water source, defecation practices, and toilet facilities Heavy rain, open defecation, waterborne V. cholerae O1Ogawa3411
Eibach et al., 2016 [37]-RainV. cholerae O1Ogawa/ El Tor496264
Emmanuel et al., 2019 [40]----83-
Endris et al., 2019 [41]Travel history, water source, contactFoodborne, waterborne, open defecation- --
Eurien et al., 2021 [42]--V. cholerae O1Ogawa4522
Eyu et al., 2022 [43]-WaterborneV. cholerae O139-55
Fagbamila et al., 2023 [44]Attending social gatherings, source of drinking water, eating habits, hygiene and sanitationWaterborne, attending social gathering----
Faruque et al., 2021 [45]Water source, toilet use pattern-- --
Feglo et al., 2018 [46]--V. cholerae O1Ogawa/ El tor6240
George et al., 2018 [47]Contact, wating habits, hygiene and sanitationWaterborne, foodborne, poor sanitationV. cholerae O1Ogawa5130
Gopalkrishna et al., 2019 [48]Water source WaterborneV. cholerae O1Ogawa/ El tor466
Goswami et al., 2019 [49]Source of drinking waterWaterborne, travel historyV. cholerae O1Ogawa/ El tor22
Golicha et al., 2018 [50]Water sources, hygiene and sanitation, eating habitsWaterborne, attending social gatheringV. cholerae O1Ogawa--
Githuku et al., 2016 [51]--V. cholerae O1Ogawa/ El Tor--
Grandesso et al., 2019 [52]Contact, water source, food consumption, type of toilet used, hygiene and sanitation,-V. cholerae O1 151116
Helou et al., 2023 [53]--V. cholerae O1---
Iramiot et al., 2019 [54]Water sources and safety, hygiene and sanitationOpen defecationV. cholerae O1Inaba7169
Issahaku et al., 2020 [55]Visit to the CTC, wash hands before eating, eating street-vended food, drinking sachet waterVisiting cholera treatment centersV. cholerae O1Ogawa--
Jain et al., 2021 [56]Water from tanks, sewage effluentWaterborne- 184
Jikal et al., 2019 [57]Water sources, hygiene and sanitation, eating habitsFoodborneV. cholerae O1Ogawa/El tor--
Jones et al., 2020 [58]-WaterborneV. cholerae O1 964372
Junejo et al., 2023 [59]Water sources Poor sanitation V. cholerae O1Ogawa--
Kanu et al., 2018 [60]Water sources, hygiene and sanitation, contact, eating habits-----
Kapata et al., 2018 [61]-Waterborne- --
Kaponda et al., 2019 [62]Source drinking waterWaterborne- --
Kateule et al., 2024 [63]-Heavy rain, waterborneV. cholerae O1Ogawa2091253
Kisera et al., 2020 [64]-overcrowding, poor sanitationV. cholerae O1Inaba3022
Kumar et al., 2022 [65]-Waterborne, open defecationV. cholerae O1Ogawa--
Kigen et al., 2020 [66]Water sources, contact, hygiene and sanitation, education, eating habits-----
Kwesiga et al., 2017 [67]Water sources, hygiene and sanitation, eating habitsWaterborneV. cholerae O1Inaba/ El Tor7861
Madulla et al., 2023 [68]Water sourceWaterborne- 452352
Matapo et al., 2016 [69]Contact, access to toilet facility, knowledge on cholera, water source, hygiene and sanitation, eating habitsWaterborneV. cholerae O1Ogawa--
Mashe et al., 2020 [70]--V. cholerae O1Ogawa371241
Matimba et al., 2022 [71]--V. cholerae O1Ogawa9997
Mbala-Kingebeni et al., 2021 [72]Water sources, hygiene and sanitation, eating habitsWaterborne--17783
McCrickard et al., 2017 [73]--V. cholerae O1-5639
Monje et al., 2020 [74]Water sources Waterborne--130124
Mukhopadhyay et al., 2019 [75]Water sources-V. cholerae O1-20463
Mwaba et al., 2018 [77]--V. cholerae O1Ogawa17062
Mwape et al., 2020 [78]--V. cholerae O1Ogawa5252
Mwenda et al., 2017 [79]-FoodborneV. cholerae O139Ogawa/ El Tor2418
Nanzaluka et al., 2020 [80]Water sources, eating habits, hygiene and sanitation, household member with cholera, household shares latrine, cholera vaccinationWaterborne, contact----
Neamin et al., 2020 [81]-- --44774054
Ngere et al., 2024 [82]Mass gathering attendanceAttending social gatheringV. cholerae O1Ogawa22478
Ngere et al., 2022 [83]-FoodborneV. cholerae O1Ogawa697
Noora et al., 2017 [85]-FoodborneV. cholerae O1---
Nsubuga et al., 2019 [86]--V. cholerae O1Inaba2521
Oguttu et al., 2017 [87]Water sourceWaterborne--106
Ohene-Adjei et al., 2017 [88]-Waterborne, foodborne, poor hygiene and sanitation, open defecation - --
Okello et al., 2019 [90]Water sourceWaterborne----
Pande et al., 2018 [91]Water sourceWaterborne--618
Qaserah et al., 2021 [93]Water sources, hygiene and sanitation, household member with cholera, household shares latrine, eating habitsWaterborne----
Roobthaisong et al., 2017 [94]--V. cholerae O166 were Ogawa/El Tor, 1 was Inaba6767
Roy et al., 2024 [95]Water source, open defecation practices, public gathering attendance, eating habits, hygiene and sanitationWaterborne- --
Sabir et al., 2023 [96]--V. cholerae O1Ogawa414414
Shah et al., 2022 [97]-WaterborneV. cholerae O1Ogawa/El Tor53
Sinyange et al., 2018 [98]Water source-V. cholerae O1Ogawa/El Tor2054925
Sule et al., 2017 [99]----222
Ujjiga et al., 2015 [101]-Wars--617525
Wang et al., 2016 [102]Eating habits, travel outside home village, treated drinking water at home, had 2 oral cholera vaccine dosesFoodborne, travel- --
Winstead et al., 2020 [103]--V. cholerae O1 --
Zahid et al., 2022 [104]--V. cholerae O1Ogawa37878
Zgheir et al., 2019 [105]Water sourceWaterborneV. cholerae O198.4% Inaba/ElTor, 1.58% Ogawa/El Tor1367505
Zhao et al., 2019 [106]-War, waterborne- --

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Figure 1. PRISMA flowchart for study selection.
Figure 1. PRISMA flowchart for study selection.
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Figure 2. Distribution of studies across various LMICs. Created with MapChart, https://www.mapchart.net/world-advanced.html, accessed on 9 October 2024.
Figure 2. Distribution of studies across various LMICs. Created with MapChart, https://www.mapchart.net/world-advanced.html, accessed on 9 October 2024.
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Figure 3. Number of cholera outbreaks by years of onset.
Figure 3. Number of cholera outbreaks by years of onset.
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Figure 4. Number of cholera cases per country. Created with MapChart, https://www.mapchart.net/world-advanced.html, accessed on 9 October 2024.
Figure 4. Number of cholera cases per country. Created with MapChart, https://www.mapchart.net/world-advanced.html, accessed on 9 October 2024.
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Figure 5. Transmission routes of cholera outbreaks by years of onset.
Figure 5. Transmission routes of cholera outbreaks by years of onset.
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Figure 6. Transmission routes of cholera outbreaks by country.
Figure 6. Transmission routes of cholera outbreaks by country.
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Figure 7. Pooled prevalence of fatalities during cholera outbreaks [12,13,14,15,16,18,20,23,24,25,26,27,29,34,36,38,39,40,41,42,43,44,49,50,51,52,53,54,55,56,58,60,61,62,63,65,66,67,68,69,70,71,73,74,76,78,80,81,82,83,84,85,86,87,88,89,92,93,95,97,98,99,100,101,102,103,104,105,106].
Figure 7. Pooled prevalence of fatalities during cholera outbreaks [12,13,14,15,16,18,20,23,24,25,26,27,29,34,36,38,39,40,41,42,43,44,49,50,51,52,53,54,55,56,58,60,61,62,63,65,66,67,68,69,70,71,73,74,76,78,80,81,82,83,84,85,86,87,88,89,92,93,95,97,98,99,100,101,102,103,104,105,106].
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Figure 8. Pooled prevalence of laboratory-confirmed cholera during outbreaks [13,14,17,19,24,25,27,29,30,31,36,37,42,43,46,47,48,49,52,54,56,58,63,64,67,68,70,71,72,73,74,75,77,78,79,81,82,83,86,87,91,94,96,97,98,99,100,104,105].
Figure 8. Pooled prevalence of laboratory-confirmed cholera during outbreaks [13,14,17,19,24,25,27,29,30,31,36,37,42,43,46,47,48,49,52,54,56,58,63,64,67,68,70,71,72,73,74,75,77,78,79,81,82,83,86,87,91,94,96,97,98,99,100,104,105].
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Figure 9. Antimicrobial resistance profiles of V. cholerae isolates (n = 799).
Figure 9. Antimicrobial resistance profiles of V. cholerae isolates (n = 799).
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Asantewaa, A.A.; Odoom, A.; Owusu-Okyere, G.; Donkor, E.S. Cholera Outbreaks in Low- and Middle-Income Countries in the Last Decade: A Systematic Review and Meta-Analysis. Microorganisms 2024, 12, 2504. https://doi.org/10.3390/microorganisms12122504

AMA Style

Asantewaa AA, Odoom A, Owusu-Okyere G, Donkor ES. Cholera Outbreaks in Low- and Middle-Income Countries in the Last Decade: A Systematic Review and Meta-Analysis. Microorganisms. 2024; 12(12):2504. https://doi.org/10.3390/microorganisms12122504

Chicago/Turabian Style

Asantewaa, Anastasia A., Alex Odoom, Godfred Owusu-Okyere, and Eric S. Donkor. 2024. "Cholera Outbreaks in Low- and Middle-Income Countries in the Last Decade: A Systematic Review and Meta-Analysis" Microorganisms 12, no. 12: 2504. https://doi.org/10.3390/microorganisms12122504

APA Style

Asantewaa, A. A., Odoom, A., Owusu-Okyere, G., & Donkor, E. S. (2024). Cholera Outbreaks in Low- and Middle-Income Countries in the Last Decade: A Systematic Review and Meta-Analysis. Microorganisms, 12(12), 2504. https://doi.org/10.3390/microorganisms12122504

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