Cholera epidemic amidst the COVID-19 pandemic in Moroto district, Uganda: Hurdles and opportunities for control

Introduction On 21st March 2020, the first COVID-19 case was detected in Uganda and a COVID-19 pandemic declared. On the same date, a nationwide lockdown was instituted in response to the pandemic. Subsequently, more cases were detected amongst the returning international travelers as the disease continued to spread across the country. On May 14th, 2020, a cholera epidemic was confirmed in Moroto district at a time when the district had registered several COVID-19 cases and was in lockdown. This study aimed to describe the cholera epidemic and response activities during the COVID-19 pandemic as well as the hurdles and opportunities for cholera control encountered during the response. Materials and methods In a cross-sectional study design, we reviewed Moroto district’s weekly epidemiological records on cholera and COVID-19 from April to July 2020. We obtained additional information through a review of the outbreak investigation and control reports. Data were analyzed and presented in frequencies, proportions, attack rates, case fatality rates, graphs, and maps. Results As of June 28th, 2020, 458 cases presenting with severe diarrhea and/or vomiting were line listed in Moroto district. The most affected age group was 15–30 years, 30.1% (138/458). The females, 59.0% [270/458], were the majority. The Case Fatality Rate (CFR) was 0.4% (2/458). Whereas home use of contaminated water following the vandalization of the only clean water source in Natapar Kocuc village, Moroto district, could have elicited the epidemic, implementing COVID-19 preventive and control measures presented some hurdles and opportunities for cholera control. The significant hurdles were observing the COVID-19 control measures such as social distancing, wearing of masks, and limited time in the community due to the need to observe curfew rules starting at 6.00 pm. The opportunities from COVID-19 measures complementary to cholera control measures included frequent hand washing, travel restrictions within the district & surrounding areas, and closure of markets. Conclusion COVID-19 preventive and control measures such as social distancing, wearing of masks, and curfew rules may be a hurdle to cholera control whereas frequent hand washing, travel restrictions within the district & surrounding areas, and closure of markets may present opportunities for cholera control. Other settings experiencing concurrent cholera and COVID-19 outbreaks can borrow lessons from this study.


Introduction
On 21 st March 2020, the first COVID-19 case was detected in Uganda and a COVID-19 pandemic declared. On the same date, a nationwide lockdown was instituted in response to the pandemic. Subsequently, more cases were detected amongst the returning international travelers as the disease continued to spread across the country. On May 14 th , 2020, a cholera epidemic was confirmed in Moroto district at a time when the district had registered several COVID-19 cases and was in lockdown. This study aimed to describe the cholera epidemic and response activities during the COVID-19 pandemic as well as the hurdles and opportunities for cholera control encountered during the response.

Materials and methods
In a cross-sectional study design, we reviewed Moroto district's weekly epidemiological records on cholera and COVID-19 from April to July 2020. We obtained additional information through a review of the outbreak investigation and control reports. Data were analyzed and presented in frequencies, proportions, attack rates, case fatality rates, graphs, and maps.

Results
As of June 28 th , 2020, 458 cases presenting with severe diarrhea and/or vomiting were line listed in Moroto district. The most affected age group was 15

Introduction
On 21 st March 2020, the first case of Coronavirus disease, 2019 (COVID-19) was detected in Uganda, the pandemic was declared in the country and a countrywide lockdown instituted [1]. In the days that followed, more COVID-19 cases were detected among returning international travelers at Entebbe International Airport. While COVID-19 Pandemic was spreading and Moroto district was under lockdown with several COVID-19 cases being confirmed, on May 14 th , 2020, a cholera epidemic was confirmed in Moroto district, Northeastern Uganda. Cholera, an acute diarrheal disease caused by ingestion of food and water contaminated with the bacterium Vibrio cholerae, remains of significant public health importance in developing countries such as Uganda [2,3]. In developed countries, cholera incidence and mortality, and other diarrheal diseases have been eliminated by providing safe drinking water and maintaining proper sanitation and hygiene [4]. Globally, an estimated 1.3 to 4 million cases and 21,000 to 143,000 deaths due to cholera occur annually [5]. In most African countries, Uganda inclusive, improvements in Water Sanitation and Hygiene (WaSH) infrastructure particularly with regard to access to safe water and sanitation facility coverage is slow, resulting in suitable conditions for repeated cholera outbreaks [6][7][8]. Consequently, cholera outbreaks have previously occurred along the western border with the Democratic Republic of Congo (DRC), the Karamoja region to the north, and Kampala City slums [9]. A cholera outbreak last occurred in Moroto district in December 2015 [10].
Even though cholera has been labeled as a predictable, preventable, and treatable disease, outbreaks continue to spread across the country, with a high number of mortalities estimated to range from 61 to 182 deaths annually [9,11]. In May 2020, a cholera epidemic was detected in Nadunget sub-county, rural part of Moroto district, Karamoja subregion. This cholera epidemic occurred when entire Uganda was under lockdown due to Corona Virus Disease 2019 (COVID-19) pandemic. Moroto district, like other districts in Uganda, was pre-occupied with observance of COVID 19 standard operating procedures such as restriction of movement, social distancing, curfew, hand washing, use of masks, and others. Whereas this was the first cholera outbreak recorded in Uganda while battling another infectious epidemic, countries like Ethiopia and Sudan both recorded cholera outbreaks during the COVID-19 era [12]. Such a cholera epidemic during the COVID-19 pandemic may pose significant challenges because as efforts are directed towards fighting the pandemic, the surveillance system as well as the health care system are paralyzed.
In Moroto district, whereas access to clean water is largely affected by issues related to climate, 73% of the population is reported to be located more than 30 minutes away from a water source. Furthermore, the use of improved sanitation facilities is as low as 11% in Moroto district [13]. With such low access to water, COVID-19 prevention and control guidelines may lead to a disruption of WASH services coinciding with restrictions of humanitarian services hence posing a great hindrance to campaigns against cholera epidemic and worsening the burden.
Henceforth, to interrupt the cholera epidemic and prevent spread within Moroto district, an epidemic was declared, and response actions initiated. This study aimed to describe the epidemic and the activities to control it amidst the COVID-19 pandemic in Moroto district, Uganda. In addition, the study examines the hurdles and opportunities encountered during the cholera epidemic control amidst the COVID-19 pandemic.

Study design
This was a cross-sectional study involving a review of weekly epidemiological records and reports on cholera and COVID-19 in Moroto district from April 2020 to June 2020.

Study settings
Moroto district is one of the nine districts that make up the Karamoja sub-region in the northeastern part of Uganda. The district lies between latitudes 1˚53'N, 3˚05'N and longitudes 333 8'E, 34˚56'E with a total area of 8,516 km 2 . The district is located about 434 kilometers by road, northeast of Kampala, Uganda's capital. Location of Moroto district and administration units (Fig 1).
The population of Moroto district is 103,432 (UNCHS August 2014). The district is inhabited by the Karimojong, a distinctive agro-pastoral herder's ethnic group which highly cherishes its traditions. Moroto district is characterized by little, scattered, and irregular rainfall resulting into patchy vegetation. Rainfall is in the range of 300 to 1200mm per year, with temperatures ranging from 20 Degree Celsius (˚C) to 32˚C.
Loputuk parish, where the outbreak was first reported, is located in Nadunget subcounty. Loputuk parish has 13 villages namely; Akwapua, Kambizi, Nachogorom, Natapar kocuc, Apetaoi, Kamera, Nadiket, Aworobu, Lokwakwa, Nangorikipi, Kalopwanya, Looi and Nasinyonoit. Similarly, the parish has 13 Local Council Ones (LCIs) and 26 Village Health Teams (VHTs). Karamojong live in manyatas (an enclosed residential area, surrounded by sharp thorns and small entry points for people and a larger entry point for cattle). One manyata has multiple families and a communal space for cattle. Natapar kocuc village in particular had 6 manyatas in total. Each manyata consisted of 10 to 15 households with 5 to 10 occupants in each household. The village dwellers are mostly nomads by nature and participate in trading local alcoholic brew named Kwete. The village members stay in small grass-thatched huts surrounding their livestock Kraal. Moroto District is only at 24.6% in hygiene levels, according to the District Water Officer, despite having 72% clean water coverage.

Case definition used
According to the Ministry of Health (MOH) of Uganda Prevention and Control guidelines of Cholera of 2017, a case of cholera should be suspected in a patient aged five years or more, presenting with dehydration or death from acute watery diarrhea [14]. A case should also be considered a cholera suspect when they are aged two years or more with acute watery diarrhea in an area where a cholera epidemic has been declared [14]. A case of cholera is confirmed when V. cholerae serogroup O1 or O139 is isolated from any patient with diarrhea [14].

Study variables
We obtained a line list including variables, namely, age of cases, sex, place of origin, date of onset of symptoms, treatment outcome (recovered or died), and presence of other medical conditions. The information extracted from the outbreak investigation reports included the status of home hygiene, water source, and availability of sanitation facilities.

Inclusion and exclusion
We included; 1) cases meeting the standard case definition for cholera as per Uganda Ministry of Health cholera prevention guidelines and 2) seen for the period April to June 2020. We excluded 3 cases who reported a diarrhea lasting more than two weeks and one bloody stool case since this was likely due to other infectious conditions.

Data collection, management and analysis
Patient quantitative data related to the epidemic was obtained from the Cholera Treatment Unit (CTU) manual case report forms that had been prepared in form of a line list. From the line list, data was abstracted using a pre-tested data abstraction form developed in EpiData Manager 4.6.2. The data was then exported to and analyzed in STATA 16.0. Data were analyzed and presented in frequencies, proportions, graphs and maps. Comparison of categories (age groups versus co-infection with malaria/ age versus sex) was made using the Chi-square test. We created maps using Arch GIS software licensed (ESRI, Redlands, California, United States of America). Shapefiles used to generate the map were from open access, the Humanitarian Data Exchange at https://data.humdata.org/. Data related to safe water, sanitation, and hygiene in the affected communities was collected through observation of the participants in their communities.

Ethical clearance
This study used data collected as part of routine Ministry of Health Surveillance and outbreak work exempted from the Institution Review Board (IRB). The proposal to conduct the study was developed and submitted to the Uganda National Health Research Organization and obtained IRB exemption (UNHRO/res/cholera/godf/17.05.2021). No personal identifying information is shared.

Description of the cholera epidemic
Starting April 29 th , 2020, there had been cases of loose stool with vomiting and with/without a fever reporting to Loputuk Health Center III. Seven out of the eight fresh stool samples sent to the Central Public Health Laboratories tested positive for V. cholera, Inaba serotype in the weekly epidemiological report dated May 11 th , 2020. The index case was a 17-year-old male patient from Natapar Kocuc village, Loputuk parish, Nadunget Sub County, who reported to the health center on April 29th, 2020, with acute watery diarrhea and severe dehydration. On May 4th, 2020, more cases with similar symptoms from the same parish as the index case also presented at Loputuk health center III. The health workers on duty that day suspected cholera. They reported to the Moroto District Health Officer, who requested fresh stool samples to be collected according to the MOH guidelines. The health workers sent the collected fresh stool samples to the Central Public Health Laboratories (CPHL) for laboratory analysis and confirmation of Vibrio cholerae. The Case Fatality Rate (CFR) in this epidemic was 0.4% (2/458).
The two deaths were a 27-year-old male and a 34-year-old male, both from Kambizi village in Nadunget sub-county.
The epidemic was characterized by different distinct epidemic waves showing a propagated or progressive epidemic pattern suggesting a person-to-person transmission with a peak at 19 cases on May 19th, 2020 (Fig 2).
Whereas all the patients (100%) presented to the health facility with severe acute diarrhea and vomiting, 94.8% (434/458) had a fever.
Most patients were female (59.0%) and aged 15-30 years (30.1%). More than 50% of the patients were also aged between 4 and 30 years. The age categories of the males were significantly different from those of females (P-value = 0.020). The proportion of females affected was significantly higher than that of males affected (59.0% versus 41.0%, P-value <0.001) ( Table 1).
The attack rates were higher in females compared to males. All the age groups were affected, but the highest attack rate occurred among elderly persons. Nadunget sub-county had the highest attack rate at 9 persons per 1000. A total of 37 villages were affected, with Natapar Kocuc (33), Aworobu (19) and Kambizi (18) recording the most cases ( Table 2). Loputuk parish had the highest attack rate at 30 cases per 1000 population, followed by Boma South with 8 cases per 1000 population and Lotirir with 6 cases per 1000 population. Parishes with no cases included Musupo, Narengenya, Lobuneit, Loyaraboth, Nakwanga, Natumukale, and Tapac.

Safe water, sanitation, and hygiene in the affected communities
Whereas in 2020, the district reports indicated a latrine coverage as low as 11% in Moroto district, there was evidence of massive open field defecation among community members in Natapar Kocuc village as well as at a new electrical station construction site which housed approximately 50 casual laborers. Regarding water sources, the village had two main water sources, one of which was a motorized solar borehole. Reports from the district office indicated that the borehole had been vandalized (battery and the inverter removed) approximately two weeks before the epidemic. The vandalized village borehole is shown in  The second water source; an ordinary borehole had been nonfunctional for about two years. Without access to safe water nearby, the community members dug out a pond at the bed of a seasonal stream through which water from upstream ran whenever it rained. The dug-out pond that served the cholera affected population of Natapar Kocuc village is shown in Fig 4. In addition, some of the community members shared water sources with their domestic animals. One such alternative water source that was shared by the community in Natapar Kocuc village is shown in Fig 5. In Natapar Kocuc village, we observed several unhygienic practices at a food market where villagers vended local brew (Kwete) and boiled meat. Such unhygienic practices included touching money and then handling food with bare hands without first washing the hands, using dirty cutleries, sharing sedge grass straws as well as calabash pots, long nails of food handlers while others continued serving at the market even when they were not in good health.
with respect to COVID-19 prevention and control standard operating procedures. The activities included airing messages such as encouraging the general public to wash their hands with soap and clean water frequently. In the same vein, organizations such as the UNICEF supported the district by providing water, sanitation, and hygiene (WASH) supplies like soap, detergents, hand sanitizers, chlorine, and handwashing stations for health facilities, families, and communities at risk. Furthermore, at the time, all public gatherings had been banned and people in public facilities were cautioned to observe the recommended social distance, to frequently and appropriately practice hand hygiene (washing hands with soap as well as use of an alcohol-based hand rub, regularly cleaning and disinfecting surfaces, such as tables and door handles among others. These, among several other hygiene response activities are also relevant for cholera prevention and control.
There was restricted access to a number of public facilities such as disco halls, places of worship, academic institutions, cinema halls and sports centers. Additionally, there was restriction of travel to new areas whereby public and non-essential private transport was banned. With the curfew instituted as well, community members wouldn't move from place to another after the stipulated movement time.
Furthermore, establishment of subcommittees to implement response activities was made possible by tapping on the already existing coordination framework of the COVID-19 response. As such, subcommittees that had already been established (community engagement & social protection, risk communication & social mobilization and leadership, stewardship, coordination & oversight) as part of the COVID-19 task force were the same committees tasked to respond to the cholera epidemic at the district level. Similarly, towards promoting awareness and advocacy on cholera and its recommended preventive measures, the community gatekeepers, traditional leaders, religious leaders and youth-led groups spreading messages on COVID-19 prevention and control used the same platform.

Hurdles for cholera investigation and control
The significant hurdles observed in control of the epidemic included the COVID-19 measures that required health workers to keep social distances, frequent use of masks, and curfew. The cholera epidemic occurred when the COVID-19 pandemic had already strained the health system due to the need to reallocate some of the staff involved in general health service delivery to COVID-19 activities. There was a challenge continuing with essential service delivery and handling cholera cases while adhering to the COVID-19 preventive measures. Furthermore, the COVID restrictions, especially lockdown and curfew, meant that response teams worked for less time and returned early. Such restrictions disrupted WASH services as well as other humanitarian services that are key components of cholera prevention and control strategies. Other hurdles such as fragile socio-economic infrastructure, inability to actively mobilize resources for cholera control as well as logistical consequences were key barriers in the response. In addition to COVID-19, some suspected cholera cases had malaria as well. Such cases had to be tested for malaria using malaria Rapid Diagnostic kit Test (mRDT) and given treatment. The other significant hurdle was co-infection with malaria. Some of the cases with malaria had a severe form of cholera which required regular monitoring, yet the human resources for health were constrained or limited. Among the cholera cases, 27.1% (124/458) were diagnosed with malaria infection by mRDT. All age groups were affected by malaria infection, but the highest positivity occurred among children between 1 and 4 years (Table 3). Lastly, the epidemic occurred during the rainfall season. The heavy rainfalls towards the end of April and May exacerbated water contamination since open defecation was common.

Discussion
This study generated important lessons for controlling cholera in similar settings facing cholera and COVID-19 epidemics. Our study shows that it is possible to observe COVID-19 restrictive measures and successfully institute cholera control measures. For instance, the measures implemented during this response controlled the epidemic. Most importantly, some of the COVID-19 measures such as hand washing, restriction of big gatherings, travel restrictions between districts were complementary to the recommended cholera control measures in the national cholera guidelines [14]. Few studies have documented the concurrent cholera epidemic-COVID-19 pandemic situation and the use of reactive oral cholera vaccination campaigns. Given that COVID-19 is an ongoing pandemic, lessons from this study could be helpful to communities faced by both cholera and COVID-19 [15]. COVID-19 is known to disrupt social services [16], reducing access to health care and ultimately increasing mortality from other illnesses [17]. In this cholera epidemic during a COVID-19 pandemic, the case fatality rate (CFR) was lower than the World Health Organization recommended standard of less than 1%. We think this low CFR was due to COVID-19 measures such as increased surveillance and referral of severe cases complementing cholera control measures as a result ofhealth system alertness that facilitated notification, communication and fast return of results.
Although COVID-19 measures reinforced cholera control, some COVID-19 measures compromised the response activities. For example, to observe the curfew imposed to restrict COVID-19, the health workers deployed to sensitize communities and carry out contact tracing returned early from the field, reducing daily individual work output. This, in turn, could have contributed to the prolongation of the cholera epidemic, as was the case in Moroto. Our finding on the effect of the COVID-19 pandemic on cholera epidemic control is different from what was found by researchers in Nigeria, where the ongoing COVID-19 pandemic worsened the cholera situation [18]. The outbreak in Nigeria may have been much worse compared to our case in Moroto because the part of Nigeria where the cholera outbreak was reported was concurrently experiencing conflicts. Areas that experience conflicts and that are highly fragile break bonds between community members yet disunity in an area jeopardizes health care methods [19].
Another important finding was that the epidemic occurred in the community following the vandalization of the community safe water source. Therefore, the local authorities need to educate the communities to safeguard facilities/ equipment provided to them for the common good. The findings in this study which attribute the cholera epidemic to the home use of unsafe water, are also supported by the Uganda Ministry of Water and Environment performance report for 2020 [20]. The report indicated that the communities in the Karamoja region and Moroto district, in particular, had 40% of water sources contaminated with E. Coli [20]. Therefore for Uganda to meet the United Nation Sustainable Development Goal target for universal safe water coverage by 2030 [21], more efforts to increase access to safe water is required.
This study also documented several bad food handling practices in the market at Natapar Kocuc village that had potential to promote the spread of cholera and other foodborne infections within the community. Since the affected population were mostly semi-nomads, we anticipate that these bad practices were not localized to Natapar Kocuc village alone but also the entire Moroto district and other places visited by the semi-nomads. Therefore, in order to prevent such unhygienic practices ultimately result in infectious disease outbreaks [22,23], the Moroto local government and the MOH will need to educate the food handlers on the safe food handling practices and also institute regular healthy fitness screening of the food handlers as well as hygiene inspections of all markets and eating places.
In addition to cholera and COVID-19, malaria infections were identified among the patients seen. These multiple infectious diseases can potentially worsen the poverty in the region through the reduction in production and diversion of resources for their treatment [24]. Thus, to address the multiple infections and malaria, the Ministry of Health will need to put more effort into better training of health care workers for appropriate diagnostic and management of patients with such co-infection in a pandemic context.
Even though a reactive oral cholera vaccination campaign was carried out during the outbreak, the decrease in the number of cases cannot be attributed to the vaccination exercise because it was evident that the outbreak was already on a declining trend at the time the first dose was administered. Much as the vaccination exercise not have been useful for controlling the outbreak, it can be useful for preventing future cholera outbreaks in the district.
This study was without some limitations. The findings shared were based on the daily line list kept at the CTU set up during response. As such, there may have been chance of non-, under or over reporting since we did not include the cases ourselves. However, since we cleaned the data and excluded the records that were not clear or had missing information, the data can support our conclusions. In addition, most of the authors also participated in the outbreak response. Therefore, they were able to identify errors in data and bring them to the attention of the broader team for the final decision.

Conclusions
Home use of contaminated water and open defecation may have elicited the community-wide cholera epidemic in Moroto district amidst the COVID-19 pandemic. COVID-19 preventive and control measures such as social distancing, wearing of masks, and curfew rules may be a hurdle to cholera control whereas frequent hand washing, travel restrictions within the district & surrounding areas, and closure of markets may present opportunities for cholera control. The response team successfully implemented cholera control activities alongside COVID-19 standard guidelines. Other settings with concurrent cholera and COVID-19 like epidemics can borrow lessons from our study.