**3. The current situation of cholera in Mozambique**

Since most publications are interconnected, based on the same campaigns and projects, they shared some constraints and limitations. They might not be explored in full depth in the following subsections. Section 5.7.3 presents more details and respective analyses on the limitations and constraints.

#### **3.1 Etiology**

*Healthcare Access - Regional Overviews*

strategy to mitigate the disease.

for the current knowledge of cholera in Mozambique.

**2. Sources and reviewing process**

of <5-year-old children, causing in average 13,105 demises per annum. Cholera's epidemiological profile is changed from epidemic to endemic due to the frequent outbreaks [6]. In general, there is a virtually countrywide epidemics every 5 years, but Nampula and Cuamba cities register annual cases [1], usually during the rainy season (December to June) [8]. According to Chissaque et al. [10], the last major outbreak was in 2015. Furthermore, some issues have been worsening the situation and raising increased concern. For instance, diarrhea-causing enteric bacteria are developing resistance to antibiotics [11], possibly because of overprescription. Cholera is endemic in Mozambique, but there is very limited research on the matter. There is little information on transmission patterns and how risk factors such as non-potable water, improper sanitation, and hygiene affect the incidence, prevalence, and severity of the disease [4, 9]; there is no local protocol for treating acute diarrhea in children, the only reference being from the World Health Organization (WHO) [4, 12, 13]; little is known about the challenges, success cases, and the extent of the impact of the struggle against cholera in Mozambique [2] and the operational cost to implement a vaccination campaign against cholera [14]. If such information gaps are filled, it will be possible to substantially improve the

Gujral et al. [15] wrote an important contribution to the overall understanding of cholera epidemiology in Mozambique up to 2013, based on the national surveillance data. Though it is a good reference for researchers and scholars, there were some updates published in at least three journal articles [9, 10, 16], reports from the United Nations [17] or other organizations, and 17 presentations [1–8, 11, 14, 18–24] at the XVI Scientific Journeys organized by the Mozambican National Institute of Health [25]. This chapter aims to summarize the contributions of such publications

The current analysis is based on updates presented during the XVI National Health Journeys, 17–20 September 2018, in Maputo City, in Mozambique. National Health Institute organized the event under the motto "Promovendo a intersectorialidade e a participação comunitária para o alcance dos Objectivos de Desenvolvimento Sustentável" [Promoting the multi-sectoral collaboration and community participation to meet the Sustainable Development Goals]. Since the beginning, in 1976, the journeys have been arguably the country's most relevant event on the matter, hosting presentations from leading health researchers in Mozambique [26].

Summaries of all presentations were then compiled to Revista Moçambicana de Ciências de Saúde [Mozambican Journal of Health Sciences]. There were 19 presentations directly or indirectly related to cholera. Some content was a follow-up of other previously published international journals, and it facilitated their interpretation. ATLAS.ti 8.1 (ATLAS.ti Scientific Software Development GmbH, Berlin, Germany) was used to analyze most information and Jamovi 0.9 (The Jamovi

Most studies on cholera in Mozambique conducted during the last decade were complementary, connected as part of a multidisciplinary approach for accompanying control campaigns led by the Ministry of Health, targeted to susceptible groups in areas where annual outbreaks occur during the rainy season [16]. At least half of the studies used data from Nampula City [23], but there were also studies in Tete, Moatize, Quelimane, Mocuba, Guruè, Metangula, Cuamba, and the country in general [1, 2, 5, 19–21]. Chissaque and Deus [20] presented, in the journeys, content

Project, Amsterdam, Netherlands) for meta-analysis when necessary.

directly related to a journal article published the same year [10].

**132**

The main causes of diarrhea in Mozambique, especially in children, are *V. cholerae,* rotavirus, *Shigella* spp., *Escherichia coli*, *Cryptosporidium* spp., and *Aeromonas* spp. [20]. At this stage, *V. cholerae* is well-known as the cholera-causing microorganism, even outside scholarly or scientific circles. Etiological studies are now focused on peculiarities or diversity of endemic strains in Mozambique, and how to rapidly distinguish cases of cholera from other forms of diarrhea, especially during emergency situations. The more accurate the diagnostic, the more appropriate the treatment.

According to Langa et al. [16], Mozambican *V. cholerae* O1 isolates from 2012 to 2014 outbreaks are genetically closely related to strains of pandemic worldwide, unlike the Indian-born found 20 years ago. Garrine et al. [9] went one step forward by analyzing how related 75 isolated were from patients in Manhiça District Hospital from the start of the millennium up to 2012 and 3 from the Komati River. They were able to reveal four unrelated genotypes and two clonal complexes with 22 genotypes by using a multilocus variable-number tandem-repeat analysis (MLVA), and through whole genome sequencing (WGS), they detected recombination and four isolates genetically unable to produce cholera toxin. The investigators were also able to deduct that Wave 3 of the seventh pandemic [27–29] remained in the area for at least 8 years, originating 67 of the isolates analyzed.

It is worth mentioning *Aeromonas* spp., as Chitio and Langa [24] demonstrated that these microorganisms cause symptoms easy to confuse with cholera's, particularly during outbreaks. They detected *Aeromonas* spp. in 30 (10.4%) of 289 samples of rectal swabs from patients with suspicion of cholera during outbreaks in 2014 and 2015. The species were *Aeromonas sobria* (57%), *Aeromonas hydrophila* (20%), *Aeromonas caviae* (13%), *Aeromonas veronii* (7%), and *Aeromonas salmonicida* ssp. *salmonicida* (3%).

#### **3.2 Risk factors and health determinants**

Environmental sanitation is important to control disease for the benefit of public health [19]. For several natural, sociopolitical, cultural, and economic reasons, Mozambique is spatially heterogeneous in terms of distribution of resources, including water, housing, their conditions [30], and certainly other features potentially affecting the transmission of cholera. Thus, one shall expect to see substantial differences in terms of risk factors and health determinants in different areas throughout the country. Yet, it is possible to draw some comparisons on how one or another factor affects the dynamics of cholera transmissibility, from different authors' points of view.

Marrufo et al. [4] evaluated water, sanitation, and hygiene in the area with more cases of cholera in Nampula City and found that 42% had improved latrines and 90% of the inhabitants had access to at least one improved water source, as defined by the World Health Organization and the United Nations Children's Fund (UNICEF) [31]: with potential to deliver safe water by nature of its design and construction. The authors did not specify their sample size (n) in the summary for the presentation, but their sample was certainly representative because they followed the guidelines of the United Nations High Commissioner for Refugees, and they were the same research team as Baltazar et al. [23] (n = 636), besides the fact that they covered a very wide area and used a statistical treatment of the data. A major health determinant is likely the lack of drainage and sewage through the entire suburban area covering six neighborhoods, particularly when it rains [4, 8, 20]. According to Ramos et al. [19], residents of Bairro Novo [New Neighborhood], Quelimane City, claimed to frequently observe human stool and trash floating when it rains and water accumulates through the streets. This area also lacks a sewage system and has a shortage of latrines.

A different research team [22] interviewed 59 patients with suspicion of cholera in the rural community of Casacone and found the same percentage as Marrufo et al. [4] of households with latrines (42%), but there were differences: 64% used well water, and none treated it before consuming. Besides the differences in the settings (suburban and rural), the study groups were fundamentally different, as Paulo et al. [22] worked with people having acute diarrhea, while Marrufo et al. [4] worked with populations from a risky area. The former group was by definition people who had contact with contaminated water; thus it is not surprising that all used untreated water, unlike the latter group.

Borges et al. [5] found that people in Metangula District (Niassa Province) prefer using untreated water from the lake, even when they have access to potable water, and they could not find any explanation, particularly because most (98%) were aware of cholera and the associated risks. Adding to that fact, Francisco and Chindia [3] stated that in this particular area, temperature and precipitation do not seem to be major health determinants, and it reinforces the idea that the issue is led by behavior. There are perhaps sociocultural or religious reasons. For instance, the Zion Christian Church is well-known in Mozambique, and it is the third largest (17.5% of the population), only surpassed by Catholicism (23.8%) and Islam (17.8%) [32]. One notable ritual of this church is the "Jordan" baptism, performed in rivers, lakes, and sometimes the sea. Such level of exposition to waterborne pathogens is highly concerning, particularly in hotspots of cholera endemism. Furthermore, virtually all over Mozambique, there are people who believe that malicious individuals intentionally created cholera to harm others [2, 6, 33]. Thus, it is important to debunk such self-destructive mentality and the resulting attitudes.

### **3.3 Epidemiology**

#### *3.3.1 Geographical distribution*

The World Health Organization [34] identifies Mozambique among the African countries most affected by cholera epidemics. In the first decade of the millennium, cholera had an incidence of 12 to 127 per 100,000 inhabitants, especially in the rainy season [20]. The variant of *V. cholerae* O1 (El Tor strains) active in the country then came from the Indian subcontinent, and it can be found, for instance, in Bangladesh

**135**

**Figure 1.**

*An Update on Cholera Studies in Mozambique DOI: http://dx.doi.org/10.5772/intechopen.88431*

it occurs every 5 years [1, 4, 22].

[16, 35]. Between 25 December 2014 and 22 March 2015, there was a sequence of outbreaks through 5 provinces and 18 districts, resulting in 7073 cases reported and 53 deaths (fatality rate was 0.7%) [17]. Genetic analyses suggest that strains found in Mozambique since 2012 are also common in several other parts of the world [16], indicating the existence of different waves of contamination converging in the country. Chitio and Langa [24] and several other presenters in the XVI National Health Journeys seemed to agree that cholera has been more widespread throughout the central and northern provinces (**Figure 1**), particularly Niassa and Nampula in the north, where outbreaks occur annually, in contrast to the rest of the country, where

*Draft of Mozambican map showing the areas where research and interventions related to cholera occurred since 2013. Image adapted from Wikimedia Commons [36] under public domain. Data was compiled from the XVI National Health Journeys [1–8, 11, 14, 18–24], Chissaque et al. [10], and Vanormelingen et al. [17].*

### *An Update on Cholera Studies in Mozambique DOI: http://dx.doi.org/10.5772/intechopen.88431*

*Healthcare Access - Regional Overviews*

system and has a shortage of latrines.

used untreated water, unlike the latter group.

ent authors' points of view.

areas throughout the country. Yet, it is possible to draw some comparisons on how one or another factor affects the dynamics of cholera transmissibility, from differ-

Marrufo et al. [4] evaluated water, sanitation, and hygiene in the area with more cases of cholera in Nampula City and found that 42% had improved latrines and 90% of the inhabitants had access to at least one improved water source, as defined by the World Health Organization and the United Nations Children's Fund (UNICEF) [31]: with potential to deliver safe water by nature of its design and construction. The authors did not specify their sample size (n) in the summary for the presentation, but their sample was certainly representative because they followed the guidelines of the United Nations High Commissioner for Refugees, and they were the same research team as Baltazar et al. [23] (n = 636), besides the fact that they covered a very wide area and used a statistical treatment of the data. A major health determinant is likely the lack of drainage and sewage through the entire suburban area covering six neighborhoods, particularly when it rains [4, 8, 20]. According to Ramos et al. [19], residents of Bairro Novo [New Neighborhood], Quelimane City, claimed to frequently observe human stool and trash floating when it rains and water accumulates through the streets. This area also lacks a sewage

A different research team [22] interviewed 59 patients with suspicion of cholera in the rural community of Casacone and found the same percentage as Marrufo et al. [4] of households with latrines (42%), but there were differences: 64% used well water, and none treated it before consuming. Besides the differences in the settings (suburban and rural), the study groups were fundamentally different, as Paulo et al. [22] worked with people having acute diarrhea, while Marrufo et al. [4] worked with populations from a risky area. The former group was by definition people who had contact with contaminated water; thus it is not surprising that all

Borges et al. [5] found that people in Metangula District (Niassa Province) prefer using untreated water from the lake, even when they have access to potable water, and they could not find any explanation, particularly because most (98%) were aware of cholera and the associated risks. Adding to that fact, Francisco and Chindia [3] stated that in this particular area, temperature and precipitation do not seem to be major health determinants, and it reinforces the idea that the issue is led by behavior. There are perhaps sociocultural or religious reasons. For instance, the Zion Christian Church is well-known in Mozambique, and it is the third largest (17.5% of the population), only surpassed by Catholicism (23.8%) and Islam (17.8%) [32]. One notable ritual of this church is the "Jordan" baptism, performed in rivers, lakes, and sometimes the sea. Such level of exposition to waterborne pathogens is highly concerning, particularly in hotspots of cholera endemism. Furthermore, virtually all over Mozambique, there are people who believe that malicious individuals intentionally created cholera to harm others [2, 6, 33]. Thus, it is important to debunk such self-destructive mentality and the resulting attitudes.

The World Health Organization [34] identifies Mozambique among the African countries most affected by cholera epidemics. In the first decade of the millennium, cholera had an incidence of 12 to 127 per 100,000 inhabitants, especially in the rainy season [20]. The variant of *V. cholerae* O1 (El Tor strains) active in the country then came from the Indian subcontinent, and it can be found, for instance, in Bangladesh

**134**

**3.3 Epidemiology**

*3.3.1 Geographical distribution*

[16, 35]. Between 25 December 2014 and 22 March 2015, there was a sequence of outbreaks through 5 provinces and 18 districts, resulting in 7073 cases reported and 53 deaths (fatality rate was 0.7%) [17]. Genetic analyses suggest that strains found in Mozambique since 2012 are also common in several other parts of the world [16], indicating the existence of different waves of contamination converging in the country.

Chitio and Langa [24] and several other presenters in the XVI National Health Journeys seemed to agree that cholera has been more widespread throughout the central and northern provinces (**Figure 1**), particularly Niassa and Nampula in the north, where outbreaks occur annually, in contrast to the rest of the country, where it occurs every 5 years [1, 4, 22].

#### **Figure 1.**

*Draft of Mozambican map showing the areas where research and interventions related to cholera occurred since 2013. Image adapted from Wikimedia Commons [36] under public domain. Data was compiled from the XVI National Health Journeys [1–8, 11, 14, 18–24], Chissaque et al. [10], and Vanormelingen et al. [17].*

Vanormelingen et al. [17] included Sofala in the list of affected provinces, and Chissaque et al. [20] mentioned *V. cholerae* among the causes of diarrhea in the country's south. The main cause is the lack of potable water and proper sanitation such as improved latrines [4], though behavioral factors also contribute to the incidence and prevalence of cholera [6, 8, 21].

In Niassa Province, the most frequent reports have arisen from in two municipalities: Metangula, where the majority of the cases occur [5], and Cuamba [1]. Besides similar causes as in Nampula City, a major risk factor for cholera contamination in Niassa is the insistence on using untreated fresh water to wash dishes, take a bath, and drink, especially the population of Metangula who live at the Niassa lakeshore [5]. In their presentation, Borges et al. [5] stated that choice of fresh water is not necessarily related to the access to potable water, as there were sufficient wells for the community.

In Nampula, the six most severely affected neighborhood cities are Carrupeia, Muatala, Murrapaniua, Mutauanha, Napipine, and Natiquiri, with 193.403 inhabitants [1, 4, 18]. Other neighborhoods under risk are Namicopo, Namutequeliua, and Belenenses, especially considering a recent observation that some residents showed very low awareness on how cholera is transmitted [6]. In this decade, the city had annual outbreaks recorded at least from 2013 to 2018 [4], and it is confirmed that an outbreak is happening as this article is being written [37], but this topic will be briefly discussed in the post-conclusion note (Section 7). There was another outbreak notified 17 November 2017 in Nampula Province, Nacarôa District [22]. The most affected areas were Munana and Casaconde neighborhoods, in the administrative area also called Nacarôa, within the district.

Zambezia was another province studied, and there were studies from cities of Quelimane, Mocuba, and Gurúè [1, 2, 19]. Vanormelingen et al. [17] added Nicoadala District. First, regarding "Bairro Novo" [New Neighborhood] in Quelimane City, Ramos et al. [19] mentioned the rapid expansion of the city, hardly complying with proper urbanization planning, thus resulting in improper sanitation and hygiene. The authors decided to investigate the frequency of waterborne diseases, including diarrheic maladies, by interviewing members of 21 households, and analyzing records from the Healthcare Center from 24 July 2014 to 2017. Cholera was mentioned among the most frequent diseases, although the authors did not specify the prevalence. In general, they included the disease among the diarrheic, with 564 cases (47.3%) in 1193 recorded in the healthcare center's registry. In Mocuba, Mesa et al. [1] analyzed 128 processes of patients carrying diarrheic diseases. Although the authors did not specify the diseases, they suspected that most had cholera considering the symptoms recorded, the fatality rate of 4% (plausible, according to the World Health Organization [38]), and the fact that there was an outbreak as they were conducting their investigation. The most affected neighborhoods were Samora Machel (33%), Marmanelo (15%), CFM (11%), carreira de tiros (10%), and Tomba de Água (8%). Carlos [2] said that various minor towns of Gurúè District have been registering outbreaks of diarrheic diseases and cholera, but in 2015 there was an outbreak in its main city, also called Gurúè.

There are other areas where cholera is endemic, but the scholarly publications from the last decade did not explore in depth the epidemiologic point of view, but they are worth mentioning. For instance, the 2015 outbreaks in the country's north and center seemed interconnected and occurred during the same period, and they reached areas including the cities of Tete, Moatize, and Sofala Province [17]. There are also studies from the south, though in different time and context. Salomão et al. [21] presented results of a 2-year study (2017–2018) related to immunization campaigns in the cities of Tete and Moatize, after an outbreak in 2017. As the outbreaks were stabilizing in the provinces mentioned so far, in Sofala it was spreading, with

**137**

*\**

**Table 1.**

*Cases of cholera recorded in the decade so far.*

*An Update on Cholera Studies in Mozambique DOI: http://dx.doi.org/10.5772/intechopen.88431*

*3.3.2 Prevalence, impact, and susceptible groups*

far of the country's reality with or without an outbreak.

value slightly higher than average in endemic areas.

three from the Komati River.

sharing.

reports from Beira City, Caia, and Nhamatanda. Manhiça District Hospital keeps isolates of cholera [9], and it reflects the history of the disease there and in the areas nearby. Garrine et al. [9] worked with these isolates in their research and added

Since most studies presented at the XVI Health Journeys were follow-ups of ongoing studies, they all tended to miss some details, and some were complementary to each other. For instance, the studies after the 2015 outbreak of cholera in Nampula explored different perspectives on the problematics [4, 6–8, 14, 18, 22, 23]. **Table 1** shows some epidemiological data recorded after 2013. These are just some examples because it would be redundant to include some papers, particularly the studies conducted in Nampula. Still, there is plenty of information worth

The studies did not explain the dynamics of how the disease is spread during non-epidemic periods because virtually all were conducted during outbreaks, or at least based on them, though it might not differ much from times of outbreak, especially because the area is endemic. Phenomena such as heavy rain and natural catastrophes certainly work as amplifiers of the disease severity by increasing people's exposition to untreated water [3, 20, 39–42]. Yet, it would be a good idea to study the risk factors and disease determinants during times of low prevalence because it would, for instance, minimize the need for researchers to work under pressure or "under budget" because of non-research-driven priorities [43], avoid panic or undesirable reactions from study subjects, and perhaps be easy to prevent outbreaks or lower considerably their impact on public health. On the other hand, outbreak investigations are crucial to ensure proper intervention. Thus, the information below represents outbreak-related scenarios but somehow the best lead so

According to **Table 1**, the country's cholera fatality rate (CFR) in 2015 was 0.7%. This value is low, within the range 0–15.8% of the Global Health Observatory (GHO) in 2016, published by the World Health Organization [38]. According to the GHO, 22 countries had CFR > 1%, and only Niger, Zimbabwe, and Congo had CFR > 5%. Even the global (1.8%) was higher than Mozambique the previous year during the outbreak. Such low fatality rate was likely due to a very fast and effective response in terms of vaccination, treatment [11, 23], and other measures such as health education and support in sanitation [8, 17]. Cholera is highly virulent but also easy to treat and there is vaccine [44]. The fatality rate observed in Nacarôa (2%) was not far from the global, and it seems reasonable to expect such kind of fluctuations in a considerably small sample. It should be also reasonable to expect a

**Author Year Area Cases of** 

*Confirmed cases/suspected cases in children recorded in healthcare institutions; ns, non-specified.*

Vanormelingen et al. [17] 2015 Countrywide 7073 53 Salência et al. [11] 2014–2017 Countrywide (6 hospitals) 19/784\* ns Dengo-Baloi et al. [18] 2016 Nampula City 44/171\* ns Paulo et al. [22] 2017 Nacarôa 135 3

**cholera**

**Deaths**

*Healthcare Access - Regional Overviews*

for the community.

incidence and prevalence of cholera [6, 8, 21].

tive area also called Nacarôa, within the district.

Vanormelingen et al. [17] included Sofala in the list of affected provinces, and Chissaque et al. [20] mentioned *V. cholerae* among the causes of diarrhea in the country's south. The main cause is the lack of potable water and proper sanitation such as improved latrines [4], though behavioral factors also contribute to the

In Niassa Province, the most frequent reports have arisen from in two municipalities: Metangula, where the majority of the cases occur [5], and Cuamba [1]. Besides similar causes as in Nampula City, a major risk factor for cholera contamination in Niassa is the insistence on using untreated fresh water to wash dishes, take a bath, and drink, especially the population of Metangula who live at the Niassa lakeshore [5]. In their presentation, Borges et al. [5] stated that choice of fresh water is not necessarily related to the access to potable water, as there were sufficient wells

In Nampula, the six most severely affected neighborhood cities are Carrupeia, Muatala, Murrapaniua, Mutauanha, Napipine, and Natiquiri, with 193.403 inhabitants [1, 4, 18]. Other neighborhoods under risk are Namicopo, Namutequeliua, and Belenenses, especially considering a recent observation that some residents showed very low awareness on how cholera is transmitted [6]. In this decade, the city had annual outbreaks recorded at least from 2013 to 2018 [4], and it is confirmed that an outbreak is happening as this article is being written [37], but this topic will be briefly discussed in the post-conclusion note (Section 7). There was another outbreak notified 17 November 2017 in Nampula Province, Nacarôa District [22]. The most affected areas were Munana and Casaconde neighborhoods, in the administra-

Zambezia was another province studied, and there were studies from cities of Quelimane, Mocuba, and Gurúè [1, 2, 19]. Vanormelingen et al. [17] added Nicoadala District. First, regarding "Bairro Novo" [New Neighborhood] in

Quelimane City, Ramos et al. [19] mentioned the rapid expansion of the city, hardly complying with proper urbanization planning, thus resulting in improper sanitation and hygiene. The authors decided to investigate the frequency of waterborne diseases, including diarrheic maladies, by interviewing members of 21 households, and analyzing records from the Healthcare Center from 24 July 2014 to 2017.

Cholera was mentioned among the most frequent diseases, although the authors did not specify the prevalence. In general, they included the disease among the diarrheic, with 564 cases (47.3%) in 1193 recorded in the healthcare center's registry. In Mocuba, Mesa et al. [1] analyzed 128 processes of patients carrying diarrheic diseases. Although the authors did not specify the diseases, they suspected that most had cholera considering the symptoms recorded, the fatality rate of 4% (plausible, according to the World Health Organization [38]), and the fact that there was an outbreak as they were conducting their investigation. The most affected neighborhoods were Samora Machel (33%), Marmanelo (15%), CFM (11%), carreira de tiros (10%), and Tomba de Água (8%). Carlos [2] said that various minor towns of Gurúè District have been registering outbreaks of diarrheic diseases and cholera,

There are other areas where cholera is endemic, but the scholarly publications from the last decade did not explore in depth the epidemiologic point of view, but they are worth mentioning. For instance, the 2015 outbreaks in the country's north and center seemed interconnected and occurred during the same period, and they reached areas including the cities of Tete, Moatize, and Sofala Province [17]. There are also studies from the south, though in different time and context. Salomão et al. [21] presented results of a 2-year study (2017–2018) related to immunization campaigns in the cities of Tete and Moatize, after an outbreak in 2017. As the outbreaks were stabilizing in the provinces mentioned so far, in Sofala it was spreading, with

but in 2015 there was an outbreak in its main city, also called Gurúè.

**136**

reports from Beira City, Caia, and Nhamatanda. Manhiça District Hospital keeps isolates of cholera [9], and it reflects the history of the disease there and in the areas nearby. Garrine et al. [9] worked with these isolates in their research and added three from the Komati River.
