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Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop (2018)

Chapter:3 Understanding Infectious Disease Transmission in Urban Built Environments

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Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
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3

Understanding Infectious Disease Transmission in Urban Built Environments

Session 1 of the workshop focused on potential social, physical, environmental, and political drivers of infectious disease transmission in the urban built environment. During the first half of the session, moderated by Maria Gloria Dominguez-Bello of New York University School of Medicine, presenters explored how infectious diseases are transmitted in urban built environments. Lee Riley, professor and head of the Infectious Diseases and Vaccinology Division at the University of California, Berkeley, discussed how characteristics of slums can contribute to adverse health outcomes. Yuguo Li, professor of mechanical engineering at the University of Hong Kong, described some of the mechanisms and implications of human exposure to microbes in urban buildings, with a focus on the three major routes of respiratory infection transmission. David Smith, professor of global health at the University of Washington, explored the migration and movement of pathogens through pathways within, into, and out of urban centers, highlighting a project that mapped the transmission of malaria using cellular phone data in Kenya.

THE INFLUENCE OF SLUMS ON POPULATION HEALTH AND MICROBIAL COMMUNITIES

Framing the issues surrounding slum health, Lee Riley, professor and head of the Infectious Diseases and Vaccinology Division at the University of California, Berkeley, noted that the topic has been on the table for more than a decade, ever since the United Nations Human Settlements Programme (UN-Habitat) released a report in 2003 describing the conditions

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

of slums worldwide (UN-Habitat, 2003). The report was the first formal documentation of issues related to urban slums, he said, and it helped to establish an official definition of urban slums, with demographic, spatial, economic, legal, and social indicators for the 1 billion slum residents worldwide at the time. He explained that the report addressed life expectancy and mortality in children under 5 years of age, access to improved water sources and sanitation, and slum upgrading and poverty reduction programs. However, the report did not address health indicators, Riley said, perhaps because measures of health burden can be difficult to assess.

Riley remarked that the term slum historically has a negative connotation, although it continues to be accepted terminology by international organizations such as the United Nations (UN). According to the UN operational definition of a slum,1 a slum is a human settlement with inadequate access to safe water, inadequate access to sanitation and other infrastructure, poor structural quality of housing, overcrowding, and insecure residential status. By that operational definition, the number of people living in slums has progressively increased over the years, Riley reported. According to a 2016 UN-Habitat report, the proportion of urban residents living in slums in developing countries has decreased, but the absolute number of people has steadily increased (UN-Habitat, 2016a).

Riley explained that in Chennai, India, and in many large cities around the world, the extremely rich and poor live in adjacent neighborhoods, with slums and luxury high-rise residential buildings standing in stark contrast to one another. Despite their proximity, he said, slum residents require a different type of health care from residents of wealthier areas. To illustrate this, he described the Paraisópolis neighborhood in São Paulo, Brazil, where a fence separates the slums from the affluent residential areas. He said that residents of both areas are affected by infectious diseases, including tuberculosis (TB), HIV/AIDS, sexually transmitted infections, influenza, sepsis, urinary tract infections, hospital infections, and pharyngitis. However, he said that residents of the slum area are additionally susceptible to diseases that rarely affect residents of the adjacent affluent area, such as leptospirosis, meningitis, hepatitis (A, B, and C), vaccine-preventable diseases, multidrug-resistant TB, rheumatic heart disease, advanced stage cervical carcinoma, and microcephaly. Quoting architect and urban planner Gita Verma, who said that “the root cause of urban slums is not in urban poverty but in urban wealth,” Riley emphasized that it is urban wealth—rather than poverty—that is determining health outcomes in the slums (Verma, 2002).

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1 The definition was created by a UN Expert Group in Nairobi in 2000.

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

Potential Contribution of Slums to Adverse Health Outcomes

To explore the science around the issue of slum health and in terms of infectious diseases, Riley examined slum-specific factors that contribute to adverse health outcomes. He framed the discussion using three components of the UN’s definition of slums: inadequate access to sanitation and other infrastructure, insecure residential status, and overcrowding.

Riley explained that, in slums, inadequate access to sanitation and other infrastructure drives multiple adverse health outcomes. Increased rat density contributes to transmission of leptospirosis and typhus, he said, and open sewers contribute to hookworm, leptospirosis, diarrhea, cholera, dengue, malaria, hepatitis, and growth retardation. He said that suboptimal schools are associated with poor health education and poor nutrition; he added that undernutrition and obesity are associated with infectious disease outcomes. He reported that inappropriate and inadequate health services both contribute to poor vaccine coverage, maternal health complications, underutilization of health services, rheumatic heart disease, suicide, drug-resistant TB, and chronic diseases, such as hypertension and diabetes. Lack of residential infrastructure, such as street lighting and public bathrooms, is linked to violence against women and intentional injuries, he added. Injuries are the biggest contributor to poor health outcomes in young adult males, he said, and if people do not die immediately of intentional injuries, they often die of infectious complications of those injuries.

Riley described how insecure residential status and overcrowding are also associated with adverse health outcomes among many slum dwellers. He explained that people with insecure residential status—people living in informal tenure without a title deed—often lack representation, which could contribute to their exclusion from health care services and from having a voice in vital decisions that affect community health outcomes. He added that people who are evicted often lack access to health care services, schooling, and employment. Many people born in slum communities are not officially registered, he said, which excludes them from health care and education services as well. Furthermore, people living in such conditions are often exposed to toxic chemicals, he said, which can lead to poisoning, respiratory diseases, and cancer. He noted that the major causes of death in developing countries are infectious diseases. Finally, he suggested that low health service utilization compounds the problem by contributing to chronic diseases; unwanted pregnancy; sexually transmitted infections, including HIV; and illnesses related to substance abuse. Riley said that overcrowding in slums also engenders a host of opportunities for transmission of diseases, including TB, respiratory diseases, pharyngitis, meningitis, scabies, superinfections of the skin, acute glomerulonephritis, rheumatic heart disease, and Zika virus infection and its congenital consequences. Riley

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

focused more closely on two diseases—rheumatic heart disease and Zika virus disease—to describe how slum conditions can drive transmission.

Rheumatic Heart Disease

Rheumatic heart disease is an immunologically mediated chronic complication of group A streptococcal pharyngitis. Past World Health Organization (WHO) estimates suggested that prevalence of the disease peaks in young adults between the ages of 24 and 35 years (WHO, 2005). However, Riley reported that studies from Brazil have suggested that the mean age of severe complications of the disease has decreased. According to a study in Salvador, the median age at which children developed congestive heart failure and stroke was 12 years (Câmara et al., 2002), and a later study reported a median age as low as 9 years (Câmara et al., 2004).

To illustrate how the diversity of microbial communities for the same disease, in the same city, can affect health interventions and outcomes, Riley described a study examining the genetic distribution of group A Streptococcus carried out in three clinics in the city of Salvador, Brazil (Tartof et al., 2010). Two of the clinics included in the study were public and predominantly served children living in urban slums (São Marcos and Quinto Centro), while the other was a private clinic (Jorge Valente). The investigators examined the genetic distribution of group A Streptococcus in children with sore throat and generated Simpson’s Diversity Index scores capturing the variation of the number of emm gene sequences at each clinic. Riley reported that the diversity index for the isolates from the children who attended the private clinic was 0.92, which is almost identical to the diversity index for high-income countries according to a systematic review of global emm type distribution (Steer et al., 2009). The diversity indices for genotypes from children treated in the two slum clinics (Quinto Centro: 0.97; São Marcos: 0.96) were similar to those found in African countries (0.981) and Pacific region countries (0.979) (Steer et al., 2009; Tartof et al., 2010).

Riley explained that the investigators also examined the proportion of group A Streptococcus isolate genotypes found at each of the clinics (Tartof et al., 2010) (see Figure 3-1). The two most common isolates at the private clinic (Jorge Valente) were emm12.0 and emm1.0, representing 36 percent of isolates; he noted these are also the two most common isolates found in high-income countries (Steer et al., 2009). He said that in the two slum clinics, emm12.0 and emm1.0 represented lower proportions (São Marcos: 21 percent; Quinto Centro: 14 percent) (Tartof et al., 2010). In comparison, those two isolates account for less than 10 percent in African regions (Steer et al., 2009). Riley highlighted these findings because emm12.0 and emm1.0 are included in the 26-valent experimental vaccine for group A

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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FIGURE 3-1 Proportion of group A Streptococcus isolate genotypes found at one private clinic (Jorge Valente) and two public clinics (Emergência São Marcos and Quinto Centro) in Salvador, Brazil.
NOTE: Orange bars are isolates that are included in the 26-valent experimental vaccine for group A Streptococcus; purple bars are isolates that are not included.
SOURCES: Riley presentation, December 12, 2017; data from Tartof et al., 2010.
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

Streptococcus. If the vaccine were administered in Salvador, said Riley, then it would be more efficacious among children in private clinics than children who attend clinics in slums. There is much discussion of disparities in living conditions, he added, but disparities exist down to the cellular level. He maintained that developing better vaccines will require better understanding of the biology of the disease.

Zika Virus Disease

Riley touched on Zika virus infection and its congenital consequences to illustrate another case of how slum conditions, such as overcrowding, inadequate safe water supply, and poor quality housing, can drive high levels of virus transmission. Mosquitoes that thrive in communities living in overcrowded conditions increase the risk of human infection, he explained, so people living in slums are more likely to be exposed to diverse virus populations than people who live in more affluent, less overcrowded areas. It is hypothesized that this may be one mechanism for the higher occurrence of the microcephaly in the congenital Zika syndrome seen among people living in slums, he added. In February 2016, WHO declared a public health emergency of international concern because of the congenital syndrome in newborns of pregnant women infected by Zika, he said, but declared an end to that status later in the same year. Brazil also declared an end to the public health emergency of the Zika epidemic in early 2017, said Riley, but he emphasized that the families of children affected by microcephaly have only just begun to deal with the consequences.

Riley concluded by arguing that we must take immediate steps to formally recognize the existence of this population and not rely solely on achieving the UN Sustainable Development Goals (SDGs). He suggested that people in positions of influence in national governments should prioritize these efforts. He called for working with the residents of slums to assess burdens of disease in slum populations and for identifying and implementing novel interventions specifically designed for slums. To develop new metrics, he suggested that precision public health research should measure the biological, sociological, and environmental determinants of disease.

HUMAN EXPOSURE TO MICROBES IN URBAN BUILDINGS

Yuguo Li, professor of mechanical engineering at the University of Hong Kong, provided an overview of the mechanisms and implications of human exposure to microbes in urban buildings. He began by introducing the three major routes of respiratory infection transmission: through the air people breathe (airborne route), through the surfaces they touch (fomite

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

route), and through other people they meet (close-contact route). He noted that this concept is centuries old.2 In an urban setting, he explained, there are a huge number of opportunities for transmission as people go about their day in their homes, on public transport, and in offices, classrooms, restaurants, shops, and theaters. He added that transmission can take place through the air in the indoor air network or through close contact with other people by touching them or talking to them, or through fomites (Gao et al., 2016). Fomites are shared surfaces that can harbor and transmit infection. Transmission can take place through short-range or long-range routes, said Li. He explained that short routes involve close contact of less than 1.5 meters with large droplets (> 100 micrometers) transmitted through the air or via direct touching. He said that long-range routes—more than 1.5 meters—involve small droplets, droplet nuclei, or aerosols (< 5 micrometers) transmitted through the air or through contact with fomites (Wei and Li, 2016).

Airborne Route of Transmission

Li explained that the airborne route of transmission involves exposure to fine droplet nuclei exhaled by another person; these droplet nuclei can travel long distances. During the severe acute respiratory syndrome (SARS) nosocomial outbreak in Hong Kong in 2003, Li and his colleagues suggested that the virus transmission was airborne, at least for that particular outbreak (Li et al., 2005). He said that it is difficult to understand why in other outbreaks the virus transmission does not appear to be airborne. Once aerosols become airborne, he added, they are affected by ventilation and airflows in indoor spaces. However, he noted that technologies exist for modern buildings to help engineers improve ventilation and airflows to mitigate transmission (Zhang and Li, 2012). While strategies are available for modern buildings, he noted, there have been few studies about the air quality in slums. He added that ventilation rate is a basic parameter that is not measured or governed by the types of laws and regulations that govern water quality, for example.

Fomite Route of Transmission

The fomite route of transmission involves exposure from touching contaminated inanimate surfaces (fomites), said Li. To illustrate how quickly a virus can be transmitted through the fomite route, he described a study

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2 Girolamo Fracastoro (1478–1553) posited that “contagion is an infection that passes from one thing to another” and suggested three routes of transmission: by direct contact, through inanimate objects, and via air.

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

that investigated an outbreak of norovirus on an airplane in 2009. Of 118 passengers on the plane, 22 became infected, the majority of whom were seated on the aisles (Kirking et al., 2010). Li outlined three possibilities as to why the aisle seat passengers had a greater infection risk through the fomite route: people touch the aisle seats more often than others; crew members have more access to those seats; and/or passengers seated in the aisle may tend to use the toilets more often, where contaminated microbes are prevalent.

Researchers are still working to understand how surfaces become contaminated, said Li. He explained that the simplest version of the fomite route is transmission of a virus from one surface to another through touching. He described a potential model for contact particle transfer that has been developed by one of his colleagues: the trap and pull-off mechanism. First, the particle is trapped by the real touch area through friction (electric contact), he said, and then the particle can be transferred to another surface, depending on which surface has the highest adhesion force. He suggested that this sort of model might potentially help engineers to develop better surfaces for avoiding particle transfer.

Li said that transmission through the fomite route is fast—as fast as the airborne route—because the so-called surface touch network grows logistically and governs this rapid transmission. He explained that after a half-day on an airplane, for example, all of the touch surfaces are connected: the first one is touched by a few people, each person can touch multiple surfaces, and each surface is touched by multiple people. Within three to five generations, all the surfaces are touched. He added that if a person moves to another space while carrying a contaminant, a new surface touch network is formulated (Lei et al., 2017).

Close-Contact Route of Transmission

Exposure through the close-contact route occurs in proximity to the index patient, explained Li. He added that this route has at least three short-range subroutes: large droplets, airborne, and surface touching, such as hand shaking, body touch, or fomite (Liu et al., 2017; Xie et al., 2007) (see Figure 3-2). He added that a virus can move from one place to another through close-contact airborne transmission, which cannot be avoided. A surgical mask can help prevent transmission of large droplets in close contact, he said, but neither general ventilation nor surgical masks can prevent close-contact airborne transmission (less than 1.5 meters). He suggested that new technology is needed to better control short-range airborne transmission.

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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FIGURE 3-2 Comparison of exposure in short-range airborne route and large droplet route, showing highest concentrations of inhaled airborne and large droplet exposures within 1.5 meters.
NOTE: m = meter; µm = micrometer.
SOURCE: Li presentation, December 12, 2017.

Potential Challenges and Knowledge Gaps

Li outlined a set of potential challenges and knowledge gaps with respect to the mechanisms and implications of human exposure to microbes in indoor buildings. For instance, “separating” a particular transmission route from a multiroute process is central to animal tests, outbreak analyses, and other purposes, but it is difficult to separate the three transmission routes (Dick et al., 1987). He added that, although it is relatively easy to separate the airborne routes, it is relatively challenging to separate close-contact routes because of the difficulty of determining the source of inhaled air. He noted that the fomite route may be easier to separate, but there is not a way to do it yet. He reported that there are no field data on indoor air networks and surface touch networks, although some data on close-contact networks have been captured. Another challenge, according to Li, is the rapid evolution of social contact that is being driven by mass travel and rapid urbanization in the built environment. Despite many studies on the microbiome, he said, there is a lack of data about how microbes actually get into mass transit environments, office environments, and homes. He suggested that better understanding of the three routes of transmission will be helpful in addressing this need for data.

Li outlined three knowledge gaps from his perspective: understanding human behavior in buildings, understanding the contribution of individual transmission routes, and the lack of mechanistic models. Addressing the

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

first gap, said Li, will require gathering more detailed data on microscale human behavior to construct models of how humans interact with each other and how they interact with surfaces in a room or building. To better understand surface touch behavior, he suggested creating detailed spatial and temporal profiles that capture data about who touches what surface, for how long (in seconds), in what sequence, with what amount of touch pressure, in what contact area, and so forth. However, he noted that there are ethical concerns to obtaining such behavioral data. He suggested that better understanding the microscale will require new technology, such as rapid indoor positioning systems, body part recognition, and surface recognition systems.

The second gap highlighted by Li is the lack of data and knowledge on the individual route contribution to infection. He suggested identifying effective study designs to carry out individual route studies or human challenge investigations and noted that a number of ferret studies on airborne transmission in the recent literature were unable to demonstrate that large droplet and airborne transmission are separated (Belser et al., 2016; Herfst et al., 2012). He explained that ferret cage studies make it almost impossible to separate out close contact and questioned whether it would be possible to design a better human challenge study. The third gap Li identified was the lack of mechanistic-based pandemic models that could be used to predict the effect of different interventions, to inform policy, and to analyze outbreaks. He attributed this gap to the lack of data on parameters, such as surface survival, fomite-hand transfer rates, dose-response parameters, nose/eye touching frequency, and building data, such as window/door openings.

PATHWAYS OF PATHOGEN TRANSMISSION IN URBAN CENTERS

David Smith, professor of global health at the University of Washington, explored several pathways through which pathogens can be transmitted within, into, and out of urban centers. He noted humans in particular generally carry cell phones with them when they move around, enabling measurement of how often and how far people move. He explained that every time a person makes or receives a call or adds money to their phone, or when their phone pings a cell tower, that transaction is logged, creating a record of where people are at various points in time. He described how cell phone data have been used to investigate pathways of pathogen transmission in Kenya, in combination with other data from the Malaria Atlas Project,3 which maps how malaria parasites are distributed in the country.

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3 The Malaria Atlas Project is available at map.ox.ac.uk (accessed March 14, 2018).

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

Mapping Malaria Transmission in Kenya

Smith’s presentation focused on a study aimed at understanding the human mobility component of malaria transmission in Kenya (Wesolowski et al., 2012). He described how the investigators were able to collect call data records from 15 million anonymized cell phone users in Kenya over approximately 1 year. He explained that around 12,000 cell towers are scattered across Kenya, with most of the users being served by a single cell phone company that facilitated the data collection. He described how the investigators mapped the country’s urban areas, densely inhabited buffer settlements surrounding urban areas, and cell tower locations, and then assigned each region a relative risk for malaria. The mode of each unique user’s identifier was considered that user’s home location, he said, which was used to determine how often users moved away from home and where they moved.

The investigators also tried to map a network of people’s contacts at the country level, Smith said. He explained that, to simplify the task of dealing with such a massive and complex data set, the investigators tried to identify communities. Within a network concept, he said, people who belong to the same community tend to be more closely connected to other people in that community than they are to anyone outside that community. The map was then further enriched by assigning colors to cell towers that represented community membership, he added. All of these data were used to map the strongest networks of connections in the country, Smith continued. Nairobi is the hub of all travel in Kenya and occupies a central role in the map, he said, noting that big cities tend to structure the way people move around the country. He added that there are smaller hubs of travel in the country, such as Lake Victoria, central areas north of Nairobi, and along the coast between Nairobi and Mombasa. Smith described how the investigators used the data to compare the ways that people were moving around with the ways that people were moving parasites around the country, by identifying sources—places where people tend to come from—and sinks—places where people tend to go. He explained that they created a color-coded human travel map to compare to the known malaria parasite sources and sinks across the country.

Smith reported that after analyzing the maps, the macroscopic-level picture showed virtually no malaria transmission in Nairobi; that is, there were many parasites moving into the city, but not moving out of the city to the rest of the country. He said one reason Nairobi is a popular city to live is because it does not play a dominant role in malaria transmission, compared to Lake Victoria, which is a source of malaria transmission that exports malaria to the rest of Kenya. Smith explained that malaria moves in two ways: people visiting endemic areas may become infected during their

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
images
FIGURE 3-3 Travel networks of humans and parasites between settlements and regions in Kenya.
Left: Average monthly parasite importation by returning residents, by region.
Right: Average monthly parasite importation by visitors.
NOTES: Regions near Lake Victoria (LV), in Nairobi (N), in the central areas (Cen), and along the coast (C) are labeled accordingly. Nodes are numbered and shaded to correspond to 1 of 20 risk regions; however, nodes may share a geographic label but be shaded differently according to risk region. Arrows indicate direction of human or parasite movement from primary settlements to visited settlements.
SOURCES: Smith presentation, December 12, 2017; Wesolowski et al., 2012. From Wesolowski, A., N. Eagle, A. Tatem, D. Smith, A. Noor, R. W. Snow, and C. O. Buckee. 2012. Quantifying the impact of human mobility on malaria. Science 338(6104):267–270. Reprinted with permission from the American Association for the Advancement of Science.

stay and carry parasites back to their home, or infected people can carry the parasites with them when they visit other places, which can potentially contribute to onward infection if the destination is receptive to transmission. The investigators calculated a measure of risk using an estimate of the proportion of people who are infected, he added, as well as a measure of the number of people traveling from Nairobi, getting infected, and bringing it home. He used Figure 3-3 to illustrate how Nairobi imports malaria from many different places, particularly the areas around Lake Victoria (Figure 3-3 left); however, people traveling to Nairobi are not being infected at all (Figure 3-3 right). According to Smith, the predominant reason for these findings is that Nairobi does not have many anopheline mosquitos, the vector for malaria, for ecological reasons. He added that Nairobi has had anopheline vectors in the past as evidenced by massive malaria epidemics at the end of the previous century, so transmission is possible in Nairobi.

Shifting Vector Transmission in the Built Environment

Smith explained that there are global patterns of shifting vector transmission in urban built environments. He cited Nairobi as an example of

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

how some vector species tend to decline and disappear from urban centers, while others thrive in the same settings. Malaria prevalence tends to be much lower in urban centers, he noted. This is because of a global pattern in which cities tend to lose their anopheline vectors as they develop, he explained, but the anophelines tend to get replaced by Aedes aegypti mosquitos that can thrive in urban centers. This catalyzes a shift in the built environment away from malaria and toward dengue and arboviral transmission, which is a mounting problem in urban centers around the world. This known pattern is one of the reasons why Nairobi was immediately put on alert when Mombasa had a dengue fever outbreak, he noted. He added that this type of shift has been documented in Ecuador (Cifuentes et al., 2013).

He reported that the country saw a massive decline in malaria cases between 2001 and 2010 overall, but there was an uptick in dengue cases over the same period (he also noted that dengue did not exist in Ecuador until around 1997). As part of the malaria mapping project in Kenya, he added, the investigators analyzed mosquito-borne pathogen transmission by plotting the ratio of observed clinical cases to estimated imported infections in the city (Wesolowski et al., 2012). They found that transmission was not occurring in Kibera, one of the biggest and most well-known slums in the city, but it was occurring in the wealthier neighborhoods and suburbs where people have large green spaces and yards.

DISCUSSION

The discussion opened with Jennifer Gardy, assistant professor in the School of Population and Public Health, University of British Columbia, asking if there are slums in high-income countries, for example, in settings like a refugee camp in Calais or in Canada’s First Nations communities, such as Attawapiskat. Riley explained that it depends on which elements of the definition of slums are applied. According to the UN definition, the largest slum in the United States is located in Los Angeles, he said, and there are other communities in the United States as well as Canada and European countries that would meet certain elements of the definition of a slum. He also noted that Brazil is now considered an upper middle-income country.

Peter Daszak, president of EcoHealth Alliance, asked how slums fit into the changing patterns of cities at the macro level. Smith remarked that in the early 1980s the Guasmo Sur barrio in Guayaquil, Ecuador, was considered the biggest slum in the world, formed by poor residents squatting in the area and siphoning power from existing lines. Initially, the city governance tried to raze the area but then relented, he explained, and within 4 years, they had provided an infrastructure including roads, sewage, drainage, and metered electricity. He said that this type of transition

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
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and development can happen quickly if governments are incentivized, and it can help to mitigate infectious disease transmission.

Daszak also asked whether it would be useful to intensify research efforts for looking at fomite risks, air circulation, and pathogen transmission in slums. Li replied that there are research opportunities focusing on slums with the potential to help many people. For example, he said there have been proposals to study carbon dioxide measurements in buildings to see what is happening to the air. He added that lack of access to water for hand washing has been studied in the context of children under 5 years of age contracting respiratory infections in their homes. Riley added that he collaborates with people who do this type of work in slums, such as one researcher who studies indoor air pollution caused by cooking with biofuels in rural areas and now is applying this work to slums, but more researchers are needed. Research is currently focused on environmental exposure issues, he noted, but emphasized that it is ultimately the pathogens that determine the health outcomes. Therefore, research efforts should be focused on both issues, he added.

David Nabarro, advisor on health and sustainability at 4SD, asked three questions about studies that examine health outcomes in urban and slum settings. He first asked whether there have been comparative studies of incidence rates for specific diseases in different urban settings. Riley said that such studies are challenging to do, but he has used the health metrics, such as disability-adjusted life years (DALYs), to assess the burden of disease, particularly TB, in Rio de Janeiro. In the last census, he explained, Brazil used the UN’s definition of slums to categorize different neighborhoods as slums or nonslums, which was used to examine the relative burdens of TB. They found differences in the DALY gap, which they categorized according to gender characteristics, electricity provision in the communities, water services, sewage services, and others. This enabled them to understand with greater granularity how this disease contributes to different types of neighborhoods in the same city. He suggested that this is preferable to looking at incidence, because DALYs allow the quality of life in these communities to be quantified. However, he noted that there are not many similar studies, because they require a census to categorize communities as slums or nonslums.

Nabarro’s second question was if studies have examined the seasonality of disease incidence in the same urban setting at different times of the year. Riley replied that, although there are known seasonal patterns to different diseases, they have not yet studied seasonality of disease incidence in urban settings like Rio de Janeiro. Li reported that seasonality for influenza is being studied. He explained that seasonality involves atmospheric conditions, temperature, and humidity and surmised that indoor conditions likely determine some of those factors in the urban built environment, where

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

people spend much of their time indoors. He added that for influenza there are good data on outdoor conditions from weather monitoring stations that constantly provide data, but indoor environments are so diversified that the data are not readily available. Smith added that malaria is associated with rainfall and temperature, and it has migration-driven patterns as well as patterns driven by seasonal transmission. In Nairobi, for example, there is an uptick in malaria cases right after Christmas when people return to the city after time at home for the holidays. The pattern of seasonal migration is also a factor, he said, as people abandon their farms and move into cities to work, bringing malaria with them (see Chapter 4 for a discussion on seasonality of leptospirosis in Brazil).

Nabarro’s third question was if any studies have linked occupations of slum residents, such as rubbish picking, to health outcomes. Riley said that occupation contributes to different types of health outcomes, such as in Brazil, where leptospirosis is highly prevalent and certainly associated with occupation in some slums. For example, he said that males tend to have higher incidence of leptospirosis, probably because they spend more time outside in occupations involving exposure to contaminated bodies of water. Riley added that interpersonal injuries are major contributors to health outcomes, noting that his studies comparing TB burden in slum and nonslum communities found that the DALY gap was reversed among young adult males in Rio de Janeiro (that is, the DALY was higher among the nonslum community young adult males) (Marlow et al., 2015). He explained this unexpected reversal, despite one-quarter of all TB DALYS being associated with slum conditions, by noting that many who are incarcerated or dead due to interpersonal violence are plausibly young adult males who live in slums, and their information was not available. He said that this type of analysis can help assess what is happening on the ground in these communities beyond just infectious diseases. Li said there are data available about occupational transmission of community-acquired methicillin-resistant Staphylococcus aureus. In Hong Kong, he reported, the data show that infection rates among the estimated 200,000 to 300,000 domestic helpers in the city are quite high compared to the general community (CHP, 2007; Government of Hong Kong, 2017). In cities where foreign domestic helpers tend to do much of the housework, he said, it would be helpful to investigate infection and transmission among people who work in that sector.

Mary Wilson, clinical professor of epidemiology and biostatistics at the University of California, San Francisco, noted that during outbreaks of respiratory infections studies have identified superspreaders who are responsible for transmitting a large number of cases; she asked whether host factors, environmental conditions, or other circumstances are associated with superspreaders. Li replied that he studied superspreaders of SARS and observed that, in some outbreaks, the environment magnified the sources.

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

One of his studies analyzed the superspreading events in Singapore and Hong Kong and found that, compared to Singapore, each event in Hong Kong produced a number of infections that was an order of magnitude greater (Li et al., 2004). He noted that it is difficult to tell whether such events are because of host factors, index patients, or density of people and buildings. He added that another event occurred during the 2015 outbreak of Middle East respiratory syndrome in Seoul, Korea, when engineers neglected to install the air supply in a particular hospital room (see Chapter 4 discussion for more on the issue of superspreaders).

Eva Harris, professor of infectious diseases and director of the Center for Global Public Health at the University of California, Berkeley, commented that emerging data from Brazil and other places suggest that socioeconomic status has a large effect on microcephaly outcomes. This may be caused by such sociological factors as access to abortion, she posited, or it might be affected by other factors such as nutrition and its effect on an individual’s immune system, microbiome, and disease outcomes. Harris suggested trying to identify direct risk factors and better understand how those factors can work through the biology and the immunology to the disease outcome. Gardy suggested looking at the intergenerational effects of slums on health to consider the developmental origins of health and disease as well as how impacts on maternal health propagate to subsequent generations. For example, she suggested looking at the sequelae of children who were not raised in slums but whose parents were raised in slum environments.

Edward You, supervisory special agent in the Federal Bureau of Investigation’s Weapons of Mass Destruction Directorate, raised the issue of modern urbanization contributing to an increasingly controlled environment in which people are more immunologically naïve, which, in turn, drives increased incidence of diseases like obesity and asthma. While the focus is often on disease transmission and pathogens perturbing the system, he wondered whether the controlled environment may also be setting populations up for failure in the future. Riley noted an increase in obesity in slum communities in India and Brazil that is likely caused by changes in nutrition, including overnutrition. He said that the use of antibiotics and exposure to antibiotics in the environment, food, and water have altered the physiology of people’s bodies—such as the intestinal microbiota—in ways that contribute to diabetes and thus lead to various infectious disease health outcomes. Riley suggested studying mechanisms that influence people’s immune systems, such as the modernization of food habits, the globalization of the food trade, and the consequential changes in behavioral health and eating behavior.

Lonnie King, professor and dean emeritus at The Ohio State University College of Veterinary Medicine, remarked that food needs increase as the

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

number of people in slums and urban areas increases in real numbers. He noted that the structure of agriculture and food production is changing and moving closer as people move into urban settings, but workers are still moving back and forth between agricultural communities and cities. King suggested that this gives rise to concern about zoonotic diseases as well as foodborne illnesses.

Marcos Espinal, director of communicable diseases and health analysis at the Pan American Health Organization, asked Riley about his call for action now instead of waiting for the SDGs. He asked if there are any proposals beyond UN-Habitat’s conclusion after its conference in 2016 that the current urbanization model is costly and unsustainable, and a new agenda is needed to upgrade slum communities and address systemic issues that extend beyond health. Thomas Scott, distinguished professor in the Department of Entomology and Nematology at the University of California, Davis, added that the SDGs’ longer-term solutions are not mutually exclusive with immediate actions to improve housing, sanitation, and water supplies; he suggested finding ways to integrate both types of strategies. Riley said that the SDGs are valuable guidelines, and he is not denigrating their importance, but there are issues that need immediate action. He used the analogy of a person hit by a car: the immediate response is to help the victim, but long-term efforts should help prevent those types of accidents from occurring at all. Both types of activities are necessary, he suggested.

Dominguez-Bello posited an optimistic perspective and imagined that, in a century or two from now, the world will have at least partially solved the problem of inequities and improved the slums. But at the same time, she imagined, people will be living in crowded urban centers, while urban farms and agriculture produce food, and the human microbiome will be degraded with urbanization. She asked if urban planners and architects should be responsible for predicting and intervening against future microbial diseases in cities. Riley said he has a dark vision of the future and predicted that the issues faced by urban slums will get much worse before they improve; he said that the effect of slums on global health will be evident long before the effects of climate change and did not envision any concrete, immediate solutions. Li took a more optimistic stance, predicting that humans will be smart enough to find those solutions and create better urban centers. Smith said that his process-based perspective is focused on understanding how slums are created, how they persist, and how they go away. He predicted that those processes would not change, and there will still be slums, even if they are different types of slums.

Nabarro said that some have argued that living in an urban slum is better than living in a bad rural existence. With climate change affecting production potential in so many parts of the world, he said, movement to cities will likely increase, and slums will serve as a refuge and haven for

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×

people who are escaping real poverty in rural areas. Riley contended that urban slum populations actually fare much worse than the rural poor. He said that poverty is not necessarily related to slums, because slums have a distinct set of conditions and health outcomes. He added that aggregate data suggesting that people living in urban settings are better off are based on comparisons that are not apt. Peter Sands, executive director designate for The Global Fund to Fight AIDS, Tuberculosis and Malaria, cautioned against disaggregating urban statistics to separate slum data without disaggregating the rural statistics, because people who move to urban slums may originate from the worst parts of the rural area.

Nabarro suggested that the alternative to hoping for a future without slums is to collectively plan for the influx of people who will move to cities in search of work and opportunities. He suggested finding ways to improve slum conditions for those people, when there is often government resistance to improving infrastructure and living conditions in slums that is premised on keeping people living there from becoming permanent residents. Sands asked if there are any good models for low-cost ways to absorb large numbers of relatively poor people into a dense urban environment. Riley replied that only time will tell the effect of existing models because progress can be undercut by unpredictable political and economic circumstances—in Brazil, for example, poverty was greatly reduced during former President Lula’s tenure (2003 to 2011), but those programs are currently being rolled back, and the positive trends are reversing. Riley also cautioned that all slum communities are different, even within the same city or large slum area, and a model that works in one place may not necessarily work in another. Christopher Dye, director of strategy, policy, and information at the Office of the Director-General of WHO, remarked that there is a great deal of knowledge about what does work. For example, he explained that the Lula era contributed to a better understanding of the effectiveness of initiatives, such as community-based health insurance and cash transfer schemes. He said that the challenge is to take that knowledge of initiatives that work and implement them.

Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page19
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page21
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page23
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page24
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page25
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
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Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page27
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page28
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page29
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page30
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page31
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page32
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page33
Suggested Citation:"3 Understanding Infectious Disease Transmission in Urban Built Environments." National Academies of Sciences, Engineering, and Medicine. 2018. Urbanization and Slums: Infectious Diseases in the Built Environment: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25070.
×
Page34
Next: 4 Translating Conceptual Models of Infectious Disease Transmission and Control into Practice »
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The urban built environment is a prime setting for microbial transmission, because just as cities serve as hubs for migration and international travel, components of the urban built environment serve as hubs that drive the transmission of infectious disease pathogens. The risk of infectious diseases for many people living in slums is further compounded by their poverty and their surrounding physical and social environment, which is often overcrowded, is prone to physical hazards, and lacks adequate or secure housing and basic infrastructure, including water, sanitation, or hygiene services.

To examine the role of the urban built environment in the emergence and reemergence of infectious diseases that affect human health, the National Academies of Sciences, Engineering, and Medicine planned a public workshop. This publication summarizes the presentations and discussions from the workshop.

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