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Institute of Medicine (US) Forum on Microbial Threats. The Causes and Impacts of Neglected Tropical and Zoonotic Diseases: Opportunities for Integrated Intervention Strategies. Washington (DC): National Academies Press (US); 2011.

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The Causes and Impacts of Neglected Tropical and Zoonotic Diseases: Opportunities for Integrated Intervention Strategies.

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A15NEGLECTED TROPICAL AND ZOONOTIC DISEASES AND THEIR IMPACT ON WOMEN'S AND CHILDREN'S HEALTH

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Centers for Disease Control and Prevention25

Introduction

For the global effort to address neglected tropical diseases (NTDs) to be effective, it is essential to examine how NTDs affect the world's most vulnerable populations. Throughout the world today, a billion people are suffering from NTDs because of the heavy toll of global poverty (Hotez, 2008). Within the “bottom billion” are two populations whose biological and social realities put them at greater risk for the negative impacts of NTDs and zoonotic diseases—women and children (Figure A15-1).

A photo of a young woman with infant daughter in Papau Province, Indonesia, seeking medical care

FIGURE A15-1

Young woman with infant daughter in Papau Province, Indonesia, seeks medical care. SOURCE: Figure courtesy of Steven Stewart, CDC.

This chapter addresses neglected tropical and zoonotic diseases and their impact on women's and children's health. It considers NTDs overall, with a focus on the seven most common NTDs, which are considered “tool ready” or having an available method of prevention and control; these are the soil-transmitted helminths (STHs; hookworm, ascariasis, and trichuriasis), lymphatic filariasis, schistosomiasis, ochocerciais, and trachoma. The chapter begins by exploring some helpful constructs and models that provide the context for understanding neglected tropical and zoonotic diseases, referred to throughout as NTDs, in women and children. Next, specific ways that NTDs affect women's health and children's health are examined, followed by a discussion of NTD comorbidities and co-morbidities with other global infectious diseases of concern. The final section explores what is needed to effectively address NTDs in women and children.

Frameworks, Models, and Context

Millennium Development Goals

One of the most significant global collaborations of recent history is the effort surrounding the Millennium Development Goals (MDGs) (Figure A15-2). The MDGs are development goals for the year 2015 that were adopted by 189 United Nations (UN) Member States in 2000 (WHO, 2010). The MDGs, which were described by World Health Organization (WHO) director Margaret Chan as “the most ambitious attack on human misery in history” (Chan, 2010), are an essential reference point for examining NTDs in women and children.

A list of the eight Millennium Development Goals (MDGs)

FIGURE A15-2

The Eight Millennium Development Goals (MDGs).

The MDGs are broad and bold in scope, addressing poverty and inequality head on. They are important for understanding current global initiatives aimed at improving women's and children's health and well-being. MDGs 3–5 specifically address women's and children's well-being, including gender equality, child survival, and maternal health. MDGs 1 and 2 are about fundamental conditions that shape women's and children's health—poverty, malnutrition, and education. MDG 6 addresses the need to combat diseases that are a major source of global mortality, as well as “other diseases,” namely, neglected tropical and zoonotic diseases.

Although progress on the MDGs has been uneven (Bernstein and Hansen, 2006; UN, 2010a), the MDGs remain an indisputable international touchstone for progress, and as such offer a useful framework for reducing the burden of disease, including NTDs, in women and children.

Social Determinants of Health

As the MDGs were becoming a material force in international policy and planning, a new framework for viewing how social forces shape health was being developed and disseminated. The social determinants of health framework is rooted in decades-long discourse about achieving equity in health (Braveman, 2006; Whitehead, 1991). In the early 2000s, WHO convened a commission on the social determinants of health, which developed an analytic framework that enjoys widespread influence today (WHO, 2007). This framework lays out how fundamental social determinants of health (such as economic standing and governmental programs and policies) in turn influence intermediary determinants of health (such as access to health care) to shape individual health status, and how these forces interact in both directions to determine the health of populations. After extensive deliberation, the Commission released its findings in August 2008 in a report that recommends that global efforts to address social determinants and promote health equity do three things (WHO, 2008a):

  • Improve daily living conditions;
  • Tackle the inequitable distribution of power, money, and resources; and
  • Measure and understand the problem and assess the results of action.

The social determinants of health is a crucial framework for NTDs, because infectious disease prevention and control in the 21st century cannot be effective if limited to traditional views of the causes of disease. It must involve socially focused as well as biologically focused solutions.

Microbial Threats to Health: The Convergence Model

Another valuable construct that implicitly utilizes the social determinants of health perspective is the convergence model, developed by the Forum on Microbial Threats (IOM, 2003) (Figure A15-3). The convergence model examines the human–microbe interface in the context of an array of factors: genetic and biological; physical and environmental; ecological; and social, political, and economic. Because the convergence model is based on an analysis of infectious disease prevention and control, it is especially useful for examining NTDs and neglected zoonotic diseases in women and children. Using the convergence model, quadrant by quadrant, we explore some of the specific and unique factors that shape the realities of NTDs in women and children.

The convergence model showing the convergence factors leading to the emergence of an infectious disease

FIGURE A15-3

The convergence model. SOURCE: IOM (2003).

Applying the Convergence Model to NTDs in Women and Children

NTDs and Women and Children: Genetic and Biological Factors

Genetic and biological factors are key to understanding the impact of NTDs in women and children. Women are vulnerable because of the reproductive functions of pregnancy and childbirth, which create a range of health risks for women. Maternal mortality—defined as the death of women during pregnancy, birth, or postpartum—remains a serious problem globally. More than half a million women die in pregnancy, birth, or postpartum each year, and 99 percent of these deaths are in developing countries (WHO, 2009, p. 40). A woman in Africa may face a lifetime risk of death in pregnancy of 1 in 31, whereas the risk for women in developed regions is 1 in 4,300 (WHO et al., 2010, p. 17). NTDs exacerbate maternal health problems by causing or contributing to a number of pregnancy-related conditions (Hotez, 2009).

Women are biologically vulnerable to sexually transmitted infections (STIs), in terms of both acquisition and health impact (WHO, 2009). Women are more likely than men to have asymptomatic infections that can result in delayed diagnosis and treatment (Faro, 2001; Schmid, 2001). Women have more severe complications from STIs, including infertility, ectopic pregnancy, and increased risk of HIV (WHO, 2009). Women are vulnerable to sexual coercion and the infections that result from it (Beck-Sague et al., 2004).

Children are biologically vulnerable to infectious diseases and their impacts (Katz et al., 1998); they are exposed to microbial threats through play, work, and substandard living conditions. They are more vulnerable than adults to environmental exposures and developmental stresses, because their immune systems are not fully developed, and their developing bodies are biologically more susceptible to the effects of environmental assaults.

These vulnerabilities are central to understanding how NTDs affect women and children. For example, STHs contribute to anemia in pregnant women, jeopardizing the pregnancy and the woman's health overall. STHs in small children cause a range of health problems.

NTDs and Women and Children: Physical and Environmental Factors

Problems associated with physical and environmental factors are universal and not unique to women or children. Among such factors is the global trend toward urbanization. It is estimated that, by the year 2050, 69 percent of the world's population will live in cities (UN, 2010b). Unfortunately, the global trend toward urbanization is one that has developed hand in hand with urban poverty (Kjellstrom and Mercado, 2008). Today, 1 out of every 3 people living in a city anywhere in the world lives in a slum area (COHRE, 2008). For many women, movement to urban areas is forced by displacement from farmlands because of desertification, conflict, or widowhood. In both rural and urban areas, substandard housing, poor sanitation infrastructure, and crowding all contribute to the transmission of NTDs.

NTDs and Women and Children: Ecological Factors

Problems associated with ecological factors are also not unique to women and children, but the consequences differ. For example, women and children are 14 times more likely to die in a natural disaster than men; this is due in part to lack of self-protection skills like swimming and climbing trees (Brody et al., 2008, p. 6). In many areas of the world where NTDs are prevalent, there are limited sources of safe water for drinking, cooking, and bathing, leading to a wide range of water-related diseases and health concerns (IOM, 2009; Mara and Sleigh, 2010).

Water problems are women's problems. Women shoulder the largest burden of collecting water globally, accounting for 64 percent of water collection, as opposed to men, who perform 25 percent of water collection. Girls are engaged in 7 percent and boys 4 percent of water collection (WHO and UNICEF, 2008). The water collection task is extremely time-consuming and can expose the collector to contaminated water, infectious disease vectors, and, in regions where conflict is rife, violence.

These ecological factors contribute to NTDs in women and children. For example, a woman collecting water or washing clothes can be exposed to schistosomiasis. A child without access to safe water for drinking and bathing can contract a wide range of water-borne diseases, including schistosomiasis (Bethony et al., 2004).

NTDs and Women and Children: Social, Political, and Economic Factors

The factors with the largest impact on women and children are the social, political, and economic. Some of the social, political, and economic factors relevant to NTDs in women are poverty, illiteracy, lack of education, lack of land ownership, lack of political power, and gender inequality (Conteh et al., 2010; Okwa, 2007; RDI, 2009). Children's poverty, lack of access to health care services, and conflict and war are also factors.

Women make up the vast majority of the world's poor, its illiterate, and its landless. Women make up the largest numbers of the world's poor living on less than $1 a day (ILO, 2009; UN, 2010c). Poverty and illiteracy go hand in hand for women. Literate persons are defined as those age 15 and older who can read and write. Approximately 64 percent of illiterate people in the world are women (UNESCO, 2008). Globally about three-fourths of a billion people are illiterate, which means nearly half a billion women are illiterate (UNESCO, 2008).

Globally, a very small proportion of women—5 percent—own land (Benschop, 2004; RDI, 2009). As for women's political power, it remains limited. Women's proportion of seats on representative bodies such as parliaments is less than 23 percent for most parts of the world—9.5 percent in Arab states (IPU, 2010).

NTD prevention must bear these harsh realities in mind—for if a woman has no economic resources, has not been educated, cannot read, and does not enjoy social or political influence, she will be struggling just to survive day to day to care for her family and will not be able to focus on NTDS as a problem, even if they are deteriorating her children's and her own health. NTD prevention and education efforts must be developed with an appreciation of these conditions.

Gender Inequality

The aforementioned realities are rooted in and exacerbated by gender inequality, which is pervasive globally and is manifested in many ways (ICRW, 2005b; WEF, 2005). Gender roles create burdens (such as water collection) and limit opportunities, promoting women's poverty. Gender inequality means that women-controlled infectious disease protection is limited or non-existent. Essentially, gender inequality inhibits infectious disease prevention in women (Manderson et al., 2009). The poverty women face globally, and the limitations poverty places on women, creates conditions in which NTDs can flourish. NTDs in turn hurt women in ways that reinforce poverty, creating a cycle that must be broken.

Gender inequality supports a wide range of social policies and practices that limit women's and children's lives, opportunities, and development. These include violence against women, child marriage and child labor, and gender inequality–based practices (social practices that flow directly from systemic gender discrimination) (UNOHCHR, 2008).

Violence Against Women

A key social determinant that reinforces women's status is violence against women (DCAF, 2005). Globally, up to 6 out of 10 women experience physical and/or sexual violence in their lifetimes (UNIFEM, 2010). The prevalence of physical and/or sexual violence by a partner varies, from 15 percent in urban Japan to 71 percent in rural Ethiopia, with most areas being in the 30 to 60 percent range. Violence against women takes many forms and can include withholding, which includes aspects of food, shelter, money, etc., as well as sexual and physical assault, rape, and murder (UNIFEM, 2010). A woman who lives in fear of physical, mental, or sexual abuse faces serious challenges in taking care of her children and herself, in accessing health care, and in making life changes. Put another way, a woman facing violence is less likely to be concerned about NTDs than a woman who feels safe.

Child Marriage

Poverty plays a role in the prevalence of child marriage. In many countries—including India, Niger, and Uganda—more than half of girls are married before they turn 18. Some girls are as young as 7 or 8 years old. Once married, girls are pressured to bear children quickly, often before their bodies are ready to handle the stress of childbirth (ICRW, 2006a, 2006b, 2006c, 2006d, 2006e; Nour, 2009).

Gender Inequality–Based Practices

Gender inequality–based practices include but are not limited to so-called “honor” killings (Nasrulleh et al., 2009; UN General Assembly, 2002; UNOHCHR, 2008), dowry-related burnings (Nasrulleh and Muazzam, 2009 ; Peck et al., 2008; Sawhney, 1989), and female infanticide, defined as murder of a female infant through neglect, poison, or other maltreatment (Coale, 1991; Ferrell, 2002; Sahni et al., 2008; Sen, 1990; Srinivasan and Bedi, 2008; Sumner, 2009). These practices reinforce gender inequality and limit women's capacity to act as agents for infectious disease prevention, including the prevention of NTDs.

Children's Poverty and Child Labor

Of the 2.2 billion children in the world, 1.9 billion are living in developing countries. The number of children living in poverty is 1 billion, or every second child. Poverty plays in role in the prevalence of child marriage (UNICEF, 2005). Child poverty is rooted in limited educational opportunities and the push toward child labor. In many regions, children may be forced to work at very young ages. Globally, 7.3 percent of children ages 5–17 were engaged in hazardous work in the years 2004–2008; sub-Saharan Africa has highest incidence of child labor, where 1 in 4 children are involved (Diallo et al., 2010). Child labor exacerbates the problem of children's poverty and is detrimental to children's health; it limits children's ability to access education and thus reinforces poverty while exposing children to numerous health hazards.

Limited Health Care Services

Lack of adequate health care services has harsh consequences for women and children. Skilled care at childbirth is extremely limited in some regions, and evidence suggests that in Africa access to care in the antenatal, delivery, and postpartum period has declined in recent years (WHO, 2009). A paucity of adequate health care services in underdeveloped countries leaves many women without care for pregnancy and birth, and children without preventive services that are crucial for child survival. In terms of NTDs, this means lack of access to diagnostics, treatment, and follow-up, in addition to prevention.

Conflict, War, and Human Trafficking

Conflict and war uproot families, communities, and villages, creating large numbers of internally displaced persons in many countries, and creating waves of refugees, of which women and children are the vast majority. Conflict situations make control of infectious diseases extremely difficult, as prevention effects are thwarted by limitations on mobility and resources (Berrang-Ford et al., 2010; Beyrer et al., 2007). These conditions in turn create vulnerabilities for women and children being trafficked for sex and/or slave labor (Beyrer, 2004; Polaris Project, 2009; Willis and Levy, 2002).

What do these factors mean for the global burden of NTDs in women and children? These social determinants shape how NTDS impact women and children globally. They set up the many barriers that have led to these being widespread, devastating, and neglected diseases (Figure A15-4).

A map of the world showing the global distribution of NTDs

FIGURE A15-4

Global distribution of NTDs. SOURCE: WHO (2006). Number of neglected diseases present by country [map]. Geneva: WHO. Map produced by Public Health Mapping and GIS, Communicable Diseases, WHO (2006). Reprinted with permission from the World Health Organization. (more...)

NTDs and Women's Health

NTDs affect hundreds of millions of women in a number of ways, constituting a substantial global burden on women's health and well-being. They affect every aspect of women's lives: physical, reproductive, sexual, emotional, social, and economic. NTDs affect women's health overall, leading to a range of problems from anemia to blindness and putting women at risk for acquiring other diseases. NTDs affect women's reproductive health, including fertility, pregnancy, labor and delivery, and neonatal health (Hotez, 2009). They affect women's sexual health, increasing the risk of some sexually transmitted infections and disrupting sexual functioning. They affect women's social health by promoting exclusion and stigma (WHO, 2010). And they affect women's economic health, by affecting women's ability to work.

Each of the NTDs is unique in terms of its natural history, its known effects on human health, and the current state of the science about how it can be prevented, diagnosed, and treated. Examining the toll of trachoma, lymphatic filariasis, and schistosomiasis on women's health underlines the urgency of addressing NTDs for women. Examining the impact of NTDs on reproductive health offers a sobering glimpse at the implications of these diseases for future generations.

Women, Trachoma, and Blindness

Trachoma is a bacterial infection caused by Chlamydia trachomitis, spread from person to person via hands and clothing and by flies that carry the bacterium. Some 84 million people are infected worldwide, and 1 million women are blinded by trachoma each year (Carter Center, 2009; WHO, 2009).

Women's gender-proscribed roles as caregivers are directly related to their increased risk of acquiring trachoma and becoming blinded by it. Trachoma disproportionately affects women because women get infected in the course of caring for infected children, who may be swarmed with flies that carry the disease (APPMG, 2008/2009; IOM, 2009) (Figure A15-5). Women are two to three times more likely than men to be permanently blinded by the disease, because women have greater exposure and less access to treatment and care (Carter Center, 2009; Hotez, 2008).

A photo of a child swarmed with flies which cause infection leading to trachoma

FIGURE A15-5

Child swarmed with flies, which cause infection leading to trachoma. SOURCE: APPMG, (2008/2009). In The Neglected Tropical Diseases: A challenge we could rise to—will we? 2008/2009 with permission from Alan Fenwick of the All-Party Group on Malaria (more...)

Blindness for women means more than not being able to see. It affects a woman's ability to earn a living and the chances of her becoming married, thus promoting poverty and decreasing opportunities for education. Blindness also affects a woman's ability to care for her children. The majority (57 percent) of the world's blind persons are women, a proportion that rises with age, as women develop cataracts but often are unable to get cataract surgery (WHO, 2009).

Women, Stigma, and Lymphatic Filariasis: “Can It Be That God Does Not Remember Me?”

Lymphatic filariasis (LF) is a vector-borne disease caused by the filarial parasite Wucherria bacrofti. LF can lead to lymphedema, a swelling of the legs and genitals. This can in turn lead to disfiguring and disabling elephantiasis, a chronic condition in which the infected person's leg grows to resemble an elephant's leg. The swollen leg can become infected with bacteria and ulcerated, requiring special care and causing decreased mobility.

LF causes extreme stigma for all affected by the disease (Wynd et al., 2007). For men, LF can lead to painful and stigmatizing enlargement of the scrotum known as hydrocele. For women, LF brings about a devastating cascade of consequences, including painful social stigma and isolation (Person et al., 2009). LF affects women's ability to support themselves, especially those engaged in agriculture, where physical demands are intense. Women who develop the disease when they are young may be kept from getting an education and are often unable to get married. Without established social networks, young women with LF may experience lifelong social disconnectedness (Person et al., 2007).

Women with LF suffer psychological distress, hopelessness, shunning, and discrimination (Okwa, 2007; Person, 2008). The despair brought on by the disease can challenge even those women with deeply held religious beliefs, as reflected in the question posed by one woman with LF: “Can it be that God does not remember me?” (Person et al., 2008, p. 349).

Women and Schistosomiasis

Schistosomiasis is a waterborne parasitic infection caused by a flatworm; the three major species are S. haematobium, S. mansoni, and S. japonicum. The infection is contracted by contact with infested waters via bathing or swimming. More than 207 million people are infected with schistosomiasis, which causes a range of serious health problems (Figure A15-6). These include damage to the bladder, liver, and intestines, as well as hematuria and anemia. In addition, it can cause chronic abdominal pain, decreased tolerance for exercise, and reduced work capacity. Schistosomiasis can be effectively treated with the drug praziquantel (PZQ).

A photo of women walking in a river in South Asia

FIGURE A15-6

Women walking in river, South Asia. SOURCE: CDC (Centers for Disease Control and Prevention) Public Health Image Library. http://phil.cdc.gov. Photo Credit: Stanley O. Foster, CDC/ World Health Organization.

Historically, efforts to address schistosomiasis primarily acknowledged the severe manifestations of the disease such as hydronephrosis, which can lead to renal failure, or bladder cancer. In recent years the disabling chronic conditions of schistosomiasis have received greater attention and focus, and research has begun to examine wide-ranging knowledge gaps (Colley and Secor, 2007; King and Dangerfield-Cha, 2008). Part of this trend has been attention to urogenital schistosomiasis in women, or female genital schistosomiasis (FGS) (Friedman et al., 2007; Nour, 2010; Poggensee et al., 1999; Rollinson, 2009; Swai et al., 2006).

Female genital schistosomiasis Schistosomiasis takes an extremely heavy toll on women. An estimated 40 million women of childbearing age suffer from schistosomiasis (Friedman et al., 2007). Schistosomal lesions of the female genital tract have been found in the ovaries, fallopian tubes, uterus, cervix, vagina, and vulva. The lesions have been associated with infertility, retarded puberty, ectopic pregnancy, anemia, miscarriage, preterm delivery, carcinoma, and higher risk for sexually transmitted diseases (Poggensee et al., 1999). FGS is associated with dyspareunia and sexual dysfunction (King and Dangerfield-Cha, 2008). Ectopic pregnancy in women with schistosomiasis is more likely to be caused by fallopian lesions (Friedman et al., 2007; Laxman et al., 2008). A cross-sectional study in Zimbabwe found an association of FGS with infertility (Kjetland et al., 2010a). Damage to the cervix by schistosomal lesions may predispose infected woman to HPV infection and possible cervical cancer (Kjetland et al., 2010b; Petry at al., 2003).

FGS and HIV/AIDS Long-standing questions exist regarding the relationship of schistosomiasis infection in girls and women and acquisition of HIV (Colley and Secor, 2007; Poggensee et al., 1999). A cross-sectional study in Zimbabwe found a threefold risk of HIV infection in women with schistosomiasis (Kjetland et al., 2006). These data and observation of the spatial overlay of HIV and schistosomiasis endemicity have prompted some to suggest that schistosomiasis treatment is a viable strategy for HIV prevention (Hotez et al., 2009; Lillerud et al., 2010; Stoever et al., 2009).

In 2009, WHO hosted a meeting on schistosomiasis and HIV risk, or more specifically about “genital schistosomiasis” (which affects both men and women) (WHO, in preparation). Increased susceptibility to HIV infection in the schistosomiasis-infected woman is biologically plausible because of breaks in the epithelial barrier and/or to immune response. While exploring ways that HIV and schistosomiasis infection may interact and influence each other, the consultation noted that the relationship between FGS and HIV is complex.

Schistosomiasis and pregnancy Concern about HIV and schistosomiasis exists hand in hand with concern about schistosomiasis in pregnancy. The number of pregnant and lactating women worldwide with schistosomiasis is unknown; in Africa, 10 million women each year have schistosomiasis during pregnancy (Friedman et al., 2007). The direct effects of the disease on pregnancy include anemia, ectopic pregnancy, miscarriage, and preterm labor, in addition to difficulties in becoming pregnant (Ajana et al., 2006; Kjetland et al., 2010a).

Because of the potential dangers of schistosomiasis in pregnancy and because women with schistosomiasis may be infected with other diseases that can be effectively treated, the inclusion of pregnant women in mass drug administration (MDA) programs has been a challenge for public health. Preventive chemotherapy, the main intervention for control of STHs, LF, schistosomiaisis, and onchocerciasis, is carried out through mass distribution of seven broad-spectrum anthelminthic medications: albendazole, diethylcarbamazine, ivermectin, levamisole, mebendazole, PZQ, and pyrantyl (WHO, 2010). The drugs' safety records for nonpregnant persons and limited side effects make their administration in a single oral dose possible without the need for individual diagnosis.

In 2002, WHO reviewed the evidence about use of PZQ in pregnancy and concluded that PZQ was safe for use in the second and third trimesters of pregnancy (WHO, 2002). Observing that women ages 18–45 living in schistosomiasis-endemic regions may spend as much as a quarter of their reproductive years pregnant and 60 percent of that time lactating; the exclusion of pregnant or lactating women from schistosomiasis MDA programs means that women go without treatment for a substantial portion of their lives (WHO, 2002, p. 11).

The WHO report also noted: “Pregnant and lactating women are as susceptible to end organ damage as anyone else. The fact that lesions may develop more rapidly than was previously thought means that delays in treatment of an infected woman until she is no longer pregnant or lactating are likely to result in major end organ morbidity” (WHO, 2002, p. 12).

Although there was no evidence of harm from PZQ when it was used during pregnancy, the lack of clinical population-based safety trials data and lack of Food and Drug Administration approval led to many countries refusing to treat adolescents and even some women of childbearing age who might be pregnant. The need for safety data was clear. The result was the development of two clinical trials for treatment of pregnant women with PZQ. The first one, in Kampala, investigated use of PZQ and/or albendazole for deworming in pregnancy; it showed no harm from PZQ but also no statistically significant benefit from treatment (Ndibazza et al., 2010). A second clinical trial is under way in the Philippines (Charles H. King, personal communication, October 17, 2010).

Reproductive Consequences of NTDs for Women

The challenges of schistosomiasis prevention and control for women underline the need for heightened attention to the numerous reproductive consequences of NTDs for women (Friedman and Acosta, 2008; Hotez, 2009). NTDs are known to contribute to maternal morbidity, to promote anemia in pregnancy, and to contribute to preterm labor, low birth weight, stillbirth, and neonatal death (Yatich et al., 2010a). NTDs can also have a negative impact on sexual health, leading to dispareunia and sexual dysfunction, and can result in infertility (King and Dangerfield-Cha, 2008).

NTDs and pregnancy Under the best of circumstances, pregnancy is a time of needed care and caution to ensure a healthy outcome; in areas where NTDs are endemic, such circumstances often do not exist. In pregnancy, a number of physiological changes take place, such as increase in blood volume, and changes in the maternal gastrointestinal and cardiovascular systems as well as the immune system (Cono et al., 2006). Because of the physiological changes of pregnancy, pregnant women are particularly susceptible to a wide range of infections (Jamieson et al., 2008; Theiler et al., 2008) and may be especially susceptible to NTDs (Adegnika et al., 2007), although not all studies have confirmed this (Herter at al., 2007). Infections in pregnancy can cause severe complications and adverse outcomes, and physiologic changes of pregnancy can alter the effectiveness of medications (Cono et al., 2006; Rasmussen et al., 2007).

Among women globally, most pregnancies are unintended and unplanned; in sub-Saharan Africa, some 14 million unintended pregnancies occur each year (Hubacher et al., 2008). Few precise assessments of the number of pregnant women with NTDs exist. An estimate of the burden of hookworm infection in pregnant women in sub-Saharan Africa utilized population estimates of 148 million women of reproductive age (defined as ages 15–49) in 2005 in sub-Saharan countries where hookworm is endemic, further estimating that 37.7 million women of reproductive age are infected with hookworm. Using live birth data from sub-Saharan Africa, it was estimated that 25.9 million women were pregnant in 2005, of whom 6.9 million were infected with hookworm (Brooker et al., 2008, p. e291).

NTDs can have a number of negative effects on pregnancy, and many pregnant women are infected with more than one NTD (Belyhun et al., 2010; Nguyen et al., 2006). The negative reproductive consequences of NTDs include ectopic pregnancy, preterm labor and low birth weight, stillbirth, postpartum hemorrhage, and small size for gestational age (Yatich et al., 2010b; Zapardiel et al., 2010).

Anemia in pregnancy is a widespread problem in the developing world (WHO, 1994). Anemia is associated with risks to pregnancy and childbirth, increasing pregnant women's risk of dying in pregnancy and the likelihood of low birth weight (Brooker et al., 2008; Kavle et al., 2008). Increased risk of anemia in pregnancy has been noted in infection with STHs (Laroque et al., 2005) and schistosomiasis (Ajana et al., 2007). These realities have led to the recommendation of regular deworming for women of childbearing age and regular inclusion of pregnant women in MDA (Brooker et al., 2008; Casey et al., 2009; Phuc et al., 2009; WHO, 1994, 1998).

Mass drug administration and pregnancy challenges The most effective strategies for prevention and control of NTDs is MDA—which has particular challenges for pregnant and lactating women. Because globally most pregnancies are not planned, and many women have serial pregnancies, practices have developed that effectively exclude many women, pregnant or not, from treatment.

For example, STHs can be treated safely in pregnancy, but pregnant women may not always receive treatment (Hotez et al., 2007). As noted above, schistosomiasis treatment in pregnancy with PZQ was recommended by WHO in 2002, but lack of pregnancy safety trials has limited its use in pregnant women to date. LF cannot be treated in pregnant women, leaving pregnant women vulnerable to LF and a potential disease reservoir, which may pose a challenge to current plans for elimination. Treatment of onchocerciasis is contraindicated in pregnant women (Okwa, 2007).

Given the mixed use and safety of drugs for NTDs in pregnant and lactating women (Table A15-1), special attention needs to be given to devising strategies for the safe and consistent inclusion of pregnant and lactating women in MDA programs whenever and wherever possible. It is also necessary to develop accurate assessments of the effect that a lack of treatment of pregnant women can have on the control of NTDs overall, which may vary by disease and region.

TABLE A15-1. MDA and Pregnancy.

TABLE A15-1

MDA and Pregnancy.

NTDs and Children's Health

NTDs are a scourge on children's health globally, damaging children's health and development in a number of ways. They also take children's lives. NTDs are often considered diseases that make people sick but do not kill them. That is not the case with children, because NTDs contribute to global child mortality (Black et al., 2010; Global Network, 2010; WHO, 2008b).

Child Health Consequences of NTDs

For children who survive and live with NTDs, there are severe health consequences (Table A15-2). An infant born to an infected mother can be low birth weight, which can jeopardize the infant's chances of survival, or small for gestational age. NTDs cause anemia in children and promote malnutrition (WHO, 1994).

TABLE A15-2. Selected NTDs and Children's Health and Development.

TABLE A15-2

Selected NTDs and Children's Health and Development.

NTDs also make it harder for children to fight diseases, harming their immune response. There is some evidence that NTDs in early childhood may hamper the effectiveness of vaccinations (King and Dangerfield-Cha, 2008; LaBeaud et al., 2009). NTDs also may put children at greater risk of acquiring HIV through vertical transmission as well as childhood acquisition (Borkow et al., 2007; Gallagher et al., 2005; Secor, 2006). Evidence also suggests that NTDs may put children at heightened risk for malaria (Brooker et al., 2007; Hotez, 2008).

The STHs ascariasis, trichuriasis, and hookworm are the most common NTDs among children and are a major cause of child morbidity globally (Bethony et al., 2006). STHs are a widely recognized cause of anemia in children (Knopp et al., 2010). Hookworm causes malnutrition when the intensity of infection causes blood loss and iron deficiency anemia (Smith and Brooker, 2010). Ascaris worms can cause intestinal obstruction and gastrointestinal bleeding (Sangkhathat et al., 2003). Trichuris worms can cause colitis and dysentery.

Child Development and NTDs

Both STHs and schistosomiasis stunt children's physical growth and cognitive development, contributing to the toll NTDs take on physical growth and development for children globally. Children with NTDs are stunted in growth and are smaller in stature throughout childhood. Schistosomiasis can cause undernutrition, growth retardation, cognitive delays, and poor performance in school. NTDs contribute to the lifelong disabling effects of childhood diarrhea, which include growth deficits, impaired fitness, impaired cognitive function, impaired test performance, and delayed age starting school (Brooker, 2010; Guerrant et al., 2004).

NTDs are known to lead to cognitive impairment and poor school performance in children, damaging children's ability to learn and to remember (Brooker et al., 2004; Bundy and de Silva, 1998; Hotez et al., 2004). Some believe that a serious legacy of NTDs and other infectious diseases over generations is a reduced cognitive capacity in communities and geographical regions, and they believe NTDs play a role in reduced intelligence worldwide (Eppig et al., 2010).

NTDs also affect social and psychological development. A child who is infected with LF may develop hydrocele, which can be stigmatizing and isolating as well as physically uncomfortable. Poor school attendance and performance may also stigmatize children suffering from NTDs.

Although the toll of NTDs on children is devastating, there is good news for childhood NTD prevention and control (Table A15-2). Preventive chemotherapy—through school-based and community-level programs that administer MDA for STHs, schistosomiasis, and onchocerciasis—has proven effective (Hotez et al., 2007; WHO, 2010). For trachoma, the SAFE strategy (surgery, antibiotic treatment, face washing, and environmental control) is effective in preventing and controlling the disease; antibiotics can be administered as part of MDA (IOM, 2009).

Co-morbidities and NTDs in Women and Children

To speak of co-infection and co-morbidity for NTDs in women and children is a little like inquiring about the blueness of the sky. Co-infection and co-morbidity are unfortunately the norm, not the exception, in the landscape of NTDs in women and children. Many women and children are infected with more than one NTD, or “polyparasitized.” Co-infection with multiple NTDs is common in some regions of the world, and it is why the MDA strategy is a necessity (Clements et al., 2010; Molyneaux et al., 2005; Richards et al., 2006).

Co-infection of NTDs with other serious infectious diseases is also common. Malaria and STHs are a common co-infection; the interrelationship of the two infections is an important arena of research and prevention efforts (Brooker et al., 2007; Druilhe et al., 2005; Wiria et al., 2010). Co-infection with STHs and HIV is a complex infectious disease challenge (Assefa et al., 2009; Borkow et al., 2007; Fincham et al., 2003; Walson et al., 2010). How infection with STHs and malaria might affect mother-to-child transmission of HIV is yet another question for research and prevention (Gallagher et al., 2005).

Co-infection of schistosomiasis and HIV is a global concern, as the bidirectional disease effects appear to be distinct and require specific treatment and response (Secor, 2006). A growing body of evidence indicates schistosomiasis may accelerate HIV disease progression (Rollinson, 2009; Secor and Sundstrom, 2007). Indeed, this new knowledge may begin to influence strategies for global HIV prevention and control (Sawers and Stillwaggon, 2010). Research on the relationship of FGS and HIV acquisition has found that women with genital schistosomiasis lesions have a heightened risk of HIV infection (Kjetland et al., 2006). Young girls infected with schistosomiasis may develop genital lesions that damage the epithelial layer long before sexual debut, underlining the need for preventive treatment of schistosomiasis of girls in endemic areas (WHO, in preparation).

Addressing NTDs in Women and Children

It will take a great global effort to end NTDs—or at least to get to a point where they have gotten the attention they need and will no longer be deemed neglected (Hotez et al., 2007; Liese et al., 2010; Spiegel at al., 2010).

Addressing Women's Poverty

One of the essential steps in this direction is addressing women's poverty (Kristof and WuDunn, 2009; UN, 2010c). Steps in this direction must include the following:

  • universal education for girls and women (ICRW, 2005a);
  • economic development initiatives for women, such as microfinance, cooperatives, and training (Smith and Thurman, 2007);
  • ban or reversal of policies based on gender inequality (UNOHCHR, 2008);
  • enforcement of laws regarding violence against women; and
  • promotion of women's leadership in science and health.

To address poverty and the challenges of NTDs in women and children, it is necessary to understand how health is transmitted across lifetimes and generations. The cycle of opportunity or obstacles, as Paula Braveman has called it, is real and inexorable (RWJF, 2008) (Figure A15-7). Adult health is shaped by the social and economic opportunities adults face, along with the living and working conditions experienced, which in turn shape family health and well-being. Family health and well-being shape childhood health, which forms the basis of health in the adult. The global cycle of poverty and substandard living conditions is what must be broken in order to address NTDs and make them neglected no more.

A flow diagram showing the cycle of opportunity or obstacles

FIGURE A15-7

To address NTDs, the cycle of poverty must be broken. SOURCE: RWJF (2008). Copyright 2008 Robert Wood Johnson Foundation/Overcoming Obstacles to Health.

What Is Needed to Address NTDs in Women and Children?

The Forum on Microbial Threats will consider many strategies for effective prevention and control of NTDs. To ensure that these efforts meet the particular challenges of NTDs in women and children, a number of steps should be considered.

One step is to move from a global public health approach that focuses on mortality only to one that focuses on chronic and disabling diseases, directly addressing and acknowledging human suffering. In this regard, considering expanded development and use of indicators that measure the quality of life, such as quality-adjusted life-years (QALYs), may be appropriate (Dasbach and Teutsch, 2003).

NTD prevention efforts need to educate polyparasitized populations about risks for the diseases they face, to counter fatalist views, and to promote prevention. Development of NTD prevention innovations like the insecticide-treated bednets that have been such a boon for malaria prevention and control should be encouraged and supported.

It is essential that data be disaggregated by gender to improve identification of risk factors for women and girls; all too often work is based on estimates of disease burden. NTD surveillance efforts, research studies, and prevention programs should all collect data on gender (along with data on age and ethnicity) and develop gender-based analyses that can inform further research and practice.

The challenges that exist for MDA in pregnant women are many; they must be carefully considered and addressed. In order to do this, research on prevention of NTDs in pregnant women, as well as research on NTD prevention throughout women's life course, must be intensified. Similarly, research on the mechanisms through which NTDs impact children's health, and how these mechanisms can effectively be addressed, must be expanded.

Enhance Women's Role in Fighting NTDs

In all efforts, enhancing women's role in fighting NTDs should be central. One way to do this is to implement the “women-centered” focus of the Global Health Initiative as a way that promotes skill-building and leadership in women. NTD training for a wide range of health care providers, including lay providers who work directly with women, should be developed (Figure A15-8). In higher education, new NTD fellowships and other training opportunities for women and men must be developed, both to meet new prevention demands and to address the attrition of skilled NTDs professionals globally.

A photo of two women

FIGURE A15-8

Women are key to NTD prevention efforts. SOURCE: CDC (Centers for Disease Control and Prevention) Public Health Image Library. http://phil.cdc.gov. Photo Credit: Chris Zahniser, CDC.

Conclusion

The stakes for addressing NTDs in women and children are high. Ignoring NTDs or not addressing the specific ways they affect women and children is acquiescing to poverty, suffering, and despair. Preventing NTDs in women and children, on the other hand, will benefit everyone. It will help solve difficult global research and prevention questions, while improving the lives of families, communities, nations, and regions. An adage from the women's health arena is particularly relevant to the challenge of addressing NTDs in women and children:

“Improve women's health, improve the world.” (WHO, 2009, p. 89)

Acknowledgments

I am extremely grateful to Office of Heath Disparities researchers Sakina M. Jaffer and Victoria Fort for their assistance in the preparation of this manuscript. I also thank my collaborators Paula Braveman, Mark Eberhard, Peter Hotez, Charlie King, Pat Lammie, Anne Moore, Sue Montgomery, and Monica Parise, whose generous and expert consultation has been indispensable.

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25

The findings and conclusions in this publication are those of the author and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Copyright © 2011, National Academy of Sciences.
Bookshelf ID: NBK62515

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