• View in gallery

    Geographical distribution of Waorani population in the province of Orellana, in the Amazon region of Ecuador.

  • View in gallery

    Number of third doses administered.

  • 1.

    Zuckerman AJ, 1999. More than third of world's population has been infected with hepatitis B virus. BMJ 318: 1213.

  • 2.

    Purcell RH, 1994. Hepatitis viruses: changing patterns of human disease. Proc Natl Acad Sci USA 91: 24012406.

  • 3.

    Smedile A, Niro G, Rizzetto M, 1997. Hepatitis D virus. Richman DD, Whitley RJ, Hayden FG, eds. Clinical Virology. New York, NY: Churchill Livingstone, 12731284.

    • Search Google Scholar
    • Export Citation
  • 4.

    Torres JR, Mondolfi A, 1991. Protracted outbreak of severe delta hepatitis: experience in an isolated Amerindian population of the Upper Orinoco basin. Rev Infect Dis 13: 5255.

    • Search Google Scholar
    • Export Citation
  • 5.

    Hadler SC, De Monzon M, Ponzetto A, Anzola E, Rivero D, Mondolfi A, Bracho A, Francis DP, Gerber MA, Thung S, Gerin J, Maynard JE, Popper H, Purcell RH, 1984. Delta virus infection and severe hepatitis. An epidemic in the Yucpa Indians of Venezuela. Ann Intern Med 100: 339344.

    • Search Google Scholar
    • Export Citation
  • 6.

    Maddrey WC, 2000. Hepatitis B: an important public health issue. J Med Virol 61: 362366.

  • 7.

    Gomes-Gouvea MS, Soares MC, Bensabath G, de Carvalho-Mello IM, Brito EM, Souza OS, Queiroz AT, Carrilho FJ, Pinho JR, 2009. Hepatitis B virus and hepatitis delta virus genotypes in outbreaks of fulminant hepatitis (Labrea black fever) in the western Brazilian Amazon region. J Gen Virol 90: 26382643.

    • Search Google Scholar
    • Export Citation
  • 8.

    Buitrago B, Hadler SC, Popper H, Thung SN, Gerber MA, Purcell RH, Maynard JE, 1986. Epidemiologic aspects of Santa Marta hepatitis over a 40-year period. Hepatology 6: 12921296.

    • Search Google Scholar
    • Export Citation
  • 9.

    Bensabath G, Hadler SC, Soares MC, Fields H, Maynard JE, 1987. Epidemiologic and serologic studies of acute viral hepatitis in Brazil's Amazon Basin. Bull PAHO 21: 1627.

    • Search Google Scholar
    • Export Citation
  • 10.

    Torres JR, Machado IV, 1994. Special aspects of hepatitis B virus and delta virus infection in Latin America. Infect Dis Clin North Am 8: 1327.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mendez M, Arce M, Kruger H, Sanchez S, 1989. Prevalencia de marcadores serologicos de hepatitis en diversos grupos de poblacion del Peru. Bol OPS 106: 127138.

    • Search Google Scholar
    • Export Citation
  • 12.

    Mahoney FJ, 1999. Update on diagnosis, management, and prevention of hepatitis B virus infection. Clin Microbiol Rev 12: 351366.

  • 13.

    Manock SR, Kelley PM, Hyams KC, Douce R, 2000. An outbreak of fulminant hepatitis delta in the Waorani, an indigenous people of the Amazon basin of Ecuador. Am J Trop Med Hyg 63: 209213.

    • Search Google Scholar
    • Export Citation
  • 14.

    Villacres E, Villamar G, 2008. Prevalencia de hepatitis B, en hombres y mujeres entre 15 y 45 años de la población de Tiwino, provincia de Orellana, mediante determinación de antígenos de superficie, entre noviembre y diciembre del 2008. Documento de tesis presentada al Instituto Superior de Postgrado de la Facultad de Ciencias Médicas. Quito, Ecuador: Universidad Central del Ecuador.

    • Search Google Scholar
    • Export Citation
  • 15.

    Mancheno V, 2000. Cruz Roja Suiza Sucumbíos. Documento ejecutivo resumen de investigación e intervención. Mayo. Swiss Red Cross.

  • 16.

    Ministerio de Salud Pública del Ecuador, 2005. Manual de Normas Técnico: Administrativas, Métodos y Procedimientos de Vacunación y Vigilancia Epidemiológica del Programa Ampliado de Inmunizaciones (PAI). Quito, Ecuador: Ministerio de Salud Pública del Ecuador.

    • Search Google Scholar
    • Export Citation
  • 17.

    Ministerio de Salud Pública del Ecuador, 2007. Manual de Normas y Procedimientos del Sistema Integrado de Vigilancia Epidemiológica Componente Alerta Acción (SIVE–ALERTA). Quito, Ecuador: Ministerio de Salud Pública del Ecuador.

    • Search Google Scholar
    • Export Citation
  • 18.

    Pan American Health Organization (PAHO), 2005. Control of Diphtheria, Pertussis, Haemophilus influenzae Type b, and Hepatitis B: Field Guide. Washington, DC: PAHO. Available at: http://www.paho.org/english/AD/FCH/IM/fieldguide_pentavalent.pdf. Accessed April 15, 2016.

    • Search Google Scholar
    • Export Citation
  • 19.

    World Health Organization, 2004. Weekly Epidemiological Record. 79: 253264. Available at: http://www.who.int/wer/2004/en/wer7928.pdf. Accessed April 15, 2016.

    • Search Google Scholar
    • Export Citation
  • 20.

    Hepatitis B Foundation. Welcome to the Hepatitis B Foundation. Available at: http://www.hepb.org. Accessed April 15, 2016.

  • 21.

    Santos Ortiz de Villalba Juan, 1996. Los últimos Huaorani. Nuevo Rocafuerte, Ecuador: CICAME, Vicariato Apostólico de Aguarico, 224.

  • 22.

    Chen H, Chang M, Ni Y, Hsu H, Lee P, Lee C, Chen D, 1996. Seroepidemiology of hepatitis B virus infection in children. Ten years of mass vaccination in Taiwan. JAMA 276: 906908.

    • Search Google Scholar
    • Export Citation
  • 23.

    Milne A, Moyes CH, 1993. Hepatitis B vaccination of children in endemic areas. Elli R, ed. Hepatitis B Vaccine in Clinical Practice. New York, NY: Marcel Dekker Inc., 279931.

    • Search Google Scholar
    • Export Citation
  • 24.

    de la Hoz F, Perez L, Wheeler JG, Neira M, Hall AJ, 2005. Vaccine coverage with hepatitis B and other vaccines in the Colombian Amazon: do health worker knowledge and perception influence coverage? Trop Med Int Health 10: 322329.

    • Search Google Scholar
    • Export Citation
  • 25.

    Coimbra CE, Santos RV, Yoshida CF, Baptista ML, Flowers NM, do Valle AC, 1996. Hepatitis B epidemiology and cultural practices in Amerindian populations of Amazonia: the Tupi Monde and the Xavante from Brazil. Soc Sci Med 42: 17351743.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Five-Year Eradication of Hepatitis B Infection After an Outreach Immunization Program in the Waorani Population in the Ecuadorian Amazon

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  • 1 Ministerio de Salud Pública del Ecuador, Quito, Ecuador.
  • 2 Department of Public Health and Clinical Medicine, Epidemiology and Global Health, Umea University, Umea, Sweden.
  • 3 Consejería de Salud, Junta de Andalucía, Cádiz, Spain.
  • 4 Colegio de Ciencias de la Salud, Universidad San Francisco de Quito, Quito, Ecuador.

In Waorani communities of the Amazon basin of Ecuador, hepatitis B (HB) surface antigen was found in 14% of asymptomatic persons. The aim of this study was to identify the Waorani population in Ecuador and obtain an epidemiologically adequate coverage of vaccination against hepatitis B virus (HBV) among them. Between February and September 2010, three vaccination campaigns were completed as part of a collaborative activity between the Ecuadorian Ministry of Public Health and the community leaders in the intervention areas. In addition, in 10 of the 22 Waorani communities, during first contact, a questionnaire about risk factors for HBV infection was administered. A total of 16 Waorani communities were registered before the beginning of this intervention, but during the actual process, six additional communities were identified. In total, 1,251 community members were registered, 92.7% of which received all three doses of the vaccine. Among them, 83% of survey respondents reported having been vaccinated, but only 22% were able to show proof. Only 1% of respondents were intravenous drug users, whereas 22% had at least one tattoo. All self-identified as heterosexual, but only 32% reported using condoms during sexual intercourse. By March 2015, no new cases of HB were been reported in any of the Waorani communities. Herein, we report the importance of intersectoral collaboration to strengthen health interventions in an isolated population like the Waorani area.

Introduction

An estimated one-third of the global population has been exposed to the parenterally transmitted hepatitis B virus (HBV). Approximately 350 million are chronically infected and are at risk of cirrhosis and liver cancer.1 Delta or hepatitis D virus (HDV) has a similar transmission pattern,2 and depends on HBV replication products for its own replication within the human host.3

HBV and HDV are endemic in Amerindian populations4,5; however, among countries, large differences in prevalence that range from 25% to 83% are associated with ethnicity, geography, and socioeconomic factors.5,6 In particular, outbreaks have been reported in Brazil,7 Colombia,810 Peru,11 and Venezuela.4,5,12

The Huaorani or Waorani (also called Sabela, Auishiri, Auca, and Huao) is a native American population inhabiting the northwest of the Amazon, in the east of Ecuador. Their ancestral territory is located in an area of approximately 30,000 km2 between the Curaray and the Napo rivers in the Amazon rainforest. The Waorani sustains a link with some uncontacted indigenous populations that live in voluntary isolation. Currently, their territories are threatened by oil exploration and logging.

In a study conducted in the Waorani communities at the Amazon basin of Ecuador,13 hepatitis B (HB) surface antigen was found in the serum of 54% of jaundiced individuals and in 14% of asymptomatic persons. Interestingly, from 58 individuals identified with jaundice, four of the 22 Waorani communities were home to 79% of cases. In fact, it is well known that the Waorani population has the highest HB prevalence in the Amazonian region, and several cases of fatality due to liver disease progression and related complications have been reported.14,15

The aim of this study was to evaluate the impact of an adequate rate of vaccination against HBV among the Waorani population.

Subjects and Methods

The Waorani population in Ecuador is found in the Amazon rainforest, in the province of Orellana (286 km from Quito), and is distributed into three main geographical areas: Tiwino, Pompeya, and Nuevo Rocafuerte (Figure 1). An important mobilization occurs within these areas on a regular basis, either for hunting or for community activities.

Figure 1.
Figure 1.

Geographical distribution of Waorani population in the province of Orellana, in the Amazon region of Ecuador.

Citation: The American Society of Tropical Medicine and Hygiene 95, 3; 10.4269/ajtmh.16-0248

Between February and September 2010, three vaccination campaigns were completed in a collaborative activity between the Ecuadorian Ministry of Public Health and the community leaders of Tiwino, Pompeya, and Nuevo Rocafuerte.

A comprehensive outreach health team consisting of a medical doctor, a nurse, and a Waorani health worker visited the communities at a specific date and time, after a previous agreement with the community leader. Once in the community, the population was informed about the benefits of vaccination and answers were provided to questions that arose.

Ecuador has implemented the World Health Organization vaccination schedule guidelines.1618 The vaccine used for HB in adults is recombinant (Heberbiovac HB, La Habana, Cuba) and for children is conjugated absorbed (pentavalent). For children, the first dose is provided at the initial contact (newborn), the second dose after 1 month, and the third dose after 6 months. This schedule has demonstrated 95% efficacy in the prevention of HBV infection and its chronic consequences.19,20 To ensure the proper completion of the full vaccination scheme, a record of each individual's name, age, community of residency, doses received, and dates administered were maintained.

In addition, a self-directed questionnaire, regarding risk factors for HBV infection, was given to 10 randomly selected Waorani communities.

Results

A total of 22 Waorani communities were administered vaccinations, yielding 1,251 participants (Table 1). From this sample, 2.9% (N = 36) were neonates aged less than 28 days, 32.9% (N = 411) were children aged between 1 and 9 years, and the majority were people older than 12 years (64.2%; N = 804).

Table 1

Waorani communities identified in the province of Orellana, Ecuador

SectorCommunityPopulation
Francisco de OrellanaTiwino219
Bataboro136
Tobeta46
Miguaguno82
Yahuerpare56
Dikapare24
Kewerino28
Wentaro26
Nenquipare25
Apaika14
Noneno89
Bameno93
Boanamo13
Francisco de Orellana/AguaricoDikaro135
Gabaro26
Peneno28
Guillero32
Timpoca10
Iru18
Ginta6
Yarentaro32
AguaricoKawimeno113
Total 1,251

A total of 92.7% coverage was achieved in the Waorani communities. The lowest coverage was evidenced in the Kavimeno area corresponding to 75% (Figure 2). A total of 1,160 individuals completed all three doses of the vaccination scheme.

Figure 2.
Figure 2.

Number of third doses administered.

Citation: The American Society of Tropical Medicine and Hygiene 95, 3; 10.4269/ajtmh.16-0248

Risk factors determined by a survey answered by 199 participants, evidenced a low response rate from the Waorani community. They were based in Aguarico (16%) and in Francisco de Orellana (84%). Eighty-three percent reported previous vaccinations; however, only 22% of the health records indicated immunization with HB vaccine.

From those surveys, reported risk factors were the following: previous use of intravenous drugs (1%); 22% had at least one tattoo; 3% had received a blood transfusion; 7% had visited the dentist during the previous week; and 15% acknowledged receiving an intramuscular injection during the last 2 weeks. All respondents defined themselves as heterosexuals, and 32% reported using condoms during sexual intercourse. Nine percent reported sexual intercourse with sexual workers or with potentially HB-infected individuals without protection.

A follow-up of case records, community active surveillance, and active search incorporated into the implementation of prevention and education strategies by outreach services have resulted in the decrease of new cases reported in the Waorani population until March 2015.

Discussion

In recent years, the cultural autonomy and isolation of the Waorani population has been modified as a result of relationships with religious missionaries, the state, and oil companies.21 To the best of our knowledge, no comprehensive evaluation and follow-up has been reported of the HB vaccination process and follow-up in the Waorani population.2224 Furthermore, worldwide results of HBV vaccination outcomes demonstrate several burdens and challenges. For example, in Taiwan, after several years of the HB vaccination introduction, a decrease in coverage was detected; as well as in Indonesia, where coverage went to under 60% as time progressed.22 In Africa, coverage of the HB vaccine also tended to be lower in comparison to other vaccines. The reasons for these differences are unclear.23

The first field evaluation of the mass introduction of HB vaccine in endemic areas of Latin America was in the Colombian Amazon.24 In such highly endemic areas like the Waorani territories, transmission factors comprise environmental conditions and cultural practices such as exposure to bat bites, extraction of jigger fleas with knives, use of teeth to extract stings, scarification, bloodletting, piercing or tattooing, and sexual activity at an early age. Also, oral exposure via sharing of breastfeeding, premastication of food, sharing chewing tobacco, and consumption of drinks fermented with saliva have been highlighted as potential mechanisms of transmission.4,25

It is estimated that over time, substantial reductions in HBV and HDV prevalence is expected from HBV vaccination. Ecuador started a vaccination program against HB in the Amazon Basin in 1992. Children under 5 years of age and newborns were subject to receive three doses of inactivate viral HB vaccine, using a short schedule: first dose at the time of birth, second and third doses 2 months afterward. However, difficulties in reaching more remote areas were reported as a result of cold-chain issues, historic fragmentation of records that resulted from vaccination administration being undertaken by different health agencies and religious missions. These factors have impeded efforts to achieve the target coverage specified in the National Extended Program of Immunization.

Geographically isolated areas like Kewerino require approximately an 8-hour journey by river in a powered cooler followed by 4 hours on foot. Barriers to HBV also include a shortage of qualified teams. Moreover, achieving the frequency of visits needed for effective outreach to the community is also an area of concern. Less remote villages may have an indigenous nurse trained to use vaccines in refrigerated storage; however, maintaining an adequate supply of vaccines is problematic and HBV immunoglobulin vaccine is currently unavailable. Remote villages face enormous challenges in sustaining the cold chain including distribution, transportation, handling, preservation, and storage in optimal conditions of light and temperature to ensure the immunogenicity and protective efficacy of the vaccine. Clearly, timely neonatal vaccination would require substantial input of both human and financial resources combined with extensive logistical backup, in what continues to be a very challenging operating environment. Even if vaccination should result in interruption of HBV transmission, for a generation, there will be a pool of individuals at risk for HDV outbreaks as a result of persistent HBV infections.

Furthermore, a complete three-dose vaccination scheme was very difficult to achieve in the Waorani population due to the continuous mobilization within communities. Default to follow-up for subsequent doses occurred easily.

Overcoming HBV barriers in the Waorani population is one of the most important factors. Intersectoral collaboration intended to strengthen health interventions might contribute to positive outcomes. However, it has to be noted that no single strategy is perfect. For example, when the community would call together the community members for health issues, other activities such as social meetings, negotiations with oil companies, and hunting, appeared to be prioritized by some.

Following this experience, we believe that a similar vaccination approach for other vaccines (yellow fever, poliomyelitis, etc.) might improve coverage and obtain better epidemiological positive results in the Waorani population.

ACKNOWLEDGMENT

We thank the “Fundacion Alejandro Labaka” for its support in dealing with the logistical aspects of the difficult geographical access.

  • 1.

    Zuckerman AJ, 1999. More than third of world's population has been infected with hepatitis B virus. BMJ 318: 1213.

  • 2.

    Purcell RH, 1994. Hepatitis viruses: changing patterns of human disease. Proc Natl Acad Sci USA 91: 24012406.

  • 3.

    Smedile A, Niro G, Rizzetto M, 1997. Hepatitis D virus. Richman DD, Whitley RJ, Hayden FG, eds. Clinical Virology. New York, NY: Churchill Livingstone, 12731284.

    • Search Google Scholar
    • Export Citation
  • 4.

    Torres JR, Mondolfi A, 1991. Protracted outbreak of severe delta hepatitis: experience in an isolated Amerindian population of the Upper Orinoco basin. Rev Infect Dis 13: 5255.

    • Search Google Scholar
    • Export Citation
  • 5.

    Hadler SC, De Monzon M, Ponzetto A, Anzola E, Rivero D, Mondolfi A, Bracho A, Francis DP, Gerber MA, Thung S, Gerin J, Maynard JE, Popper H, Purcell RH, 1984. Delta virus infection and severe hepatitis. An epidemic in the Yucpa Indians of Venezuela. Ann Intern Med 100: 339344.

    • Search Google Scholar
    • Export Citation
  • 6.

    Maddrey WC, 2000. Hepatitis B: an important public health issue. J Med Virol 61: 362366.

  • 7.

    Gomes-Gouvea MS, Soares MC, Bensabath G, de Carvalho-Mello IM, Brito EM, Souza OS, Queiroz AT, Carrilho FJ, Pinho JR, 2009. Hepatitis B virus and hepatitis delta virus genotypes in outbreaks of fulminant hepatitis (Labrea black fever) in the western Brazilian Amazon region. J Gen Virol 90: 26382643.

    • Search Google Scholar
    • Export Citation
  • 8.

    Buitrago B, Hadler SC, Popper H, Thung SN, Gerber MA, Purcell RH, Maynard JE, 1986. Epidemiologic aspects of Santa Marta hepatitis over a 40-year period. Hepatology 6: 12921296.

    • Search Google Scholar
    • Export Citation
  • 9.

    Bensabath G, Hadler SC, Soares MC, Fields H, Maynard JE, 1987. Epidemiologic and serologic studies of acute viral hepatitis in Brazil's Amazon Basin. Bull PAHO 21: 1627.

    • Search Google Scholar
    • Export Citation
  • 10.

    Torres JR, Machado IV, 1994. Special aspects of hepatitis B virus and delta virus infection in Latin America. Infect Dis Clin North Am 8: 1327.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mendez M, Arce M, Kruger H, Sanchez S, 1989. Prevalencia de marcadores serologicos de hepatitis en diversos grupos de poblacion del Peru. Bol OPS 106: 127138.

    • Search Google Scholar
    • Export Citation
  • 12.

    Mahoney FJ, 1999. Update on diagnosis, management, and prevention of hepatitis B virus infection. Clin Microbiol Rev 12: 351366.

  • 13.

    Manock SR, Kelley PM, Hyams KC, Douce R, 2000. An outbreak of fulminant hepatitis delta in the Waorani, an indigenous people of the Amazon basin of Ecuador. Am J Trop Med Hyg 63: 209213.

    • Search Google Scholar
    • Export Citation
  • 14.

    Villacres E, Villamar G, 2008. Prevalencia de hepatitis B, en hombres y mujeres entre 15 y 45 años de la población de Tiwino, provincia de Orellana, mediante determinación de antígenos de superficie, entre noviembre y diciembre del 2008. Documento de tesis presentada al Instituto Superior de Postgrado de la Facultad de Ciencias Médicas. Quito, Ecuador: Universidad Central del Ecuador.

    • Search Google Scholar
    • Export Citation
  • 15.

    Mancheno V, 2000. Cruz Roja Suiza Sucumbíos. Documento ejecutivo resumen de investigación e intervención. Mayo. Swiss Red Cross.

  • 16.

    Ministerio de Salud Pública del Ecuador, 2005. Manual de Normas Técnico: Administrativas, Métodos y Procedimientos de Vacunación y Vigilancia Epidemiológica del Programa Ampliado de Inmunizaciones (PAI). Quito, Ecuador: Ministerio de Salud Pública del Ecuador.

    • Search Google Scholar
    • Export Citation
  • 17.

    Ministerio de Salud Pública del Ecuador, 2007. Manual de Normas y Procedimientos del Sistema Integrado de Vigilancia Epidemiológica Componente Alerta Acción (SIVE–ALERTA). Quito, Ecuador: Ministerio de Salud Pública del Ecuador.

    • Search Google Scholar
    • Export Citation
  • 18.

    Pan American Health Organization (PAHO), 2005. Control of Diphtheria, Pertussis, Haemophilus influenzae Type b, and Hepatitis B: Field Guide. Washington, DC: PAHO. Available at: http://www.paho.org/english/AD/FCH/IM/fieldguide_pentavalent.pdf. Accessed April 15, 2016.

    • Search Google Scholar
    • Export Citation
  • 19.

    World Health Organization, 2004. Weekly Epidemiological Record. 79: 253264. Available at: http://www.who.int/wer/2004/en/wer7928.pdf. Accessed April 15, 2016.

    • Search Google Scholar
    • Export Citation
  • 20.

    Hepatitis B Foundation. Welcome to the Hepatitis B Foundation. Available at: http://www.hepb.org. Accessed April 15, 2016.

  • 21.

    Santos Ortiz de Villalba Juan, 1996. Los últimos Huaorani. Nuevo Rocafuerte, Ecuador: CICAME, Vicariato Apostólico de Aguarico, 224.

  • 22.

    Chen H, Chang M, Ni Y, Hsu H, Lee P, Lee C, Chen D, 1996. Seroepidemiology of hepatitis B virus infection in children. Ten years of mass vaccination in Taiwan. JAMA 276: 906908.

    • Search Google Scholar
    • Export Citation
  • 23.

    Milne A, Moyes CH, 1993. Hepatitis B vaccination of children in endemic areas. Elli R, ed. Hepatitis B Vaccine in Clinical Practice. New York, NY: Marcel Dekker Inc., 279931.

    • Search Google Scholar
    • Export Citation
  • 24.

    de la Hoz F, Perez L, Wheeler JG, Neira M, Hall AJ, 2005. Vaccine coverage with hepatitis B and other vaccines in the Colombian Amazon: do health worker knowledge and perception influence coverage? Trop Med Int Health 10: 322329.

    • Search Google Scholar
    • Export Citation
  • 25.

    Coimbra CE, Santos RV, Yoshida CF, Baptista ML, Flowers NM, do Valle AC, 1996. Hepatitis B epidemiology and cultural practices in Amerindian populations of Amazonia: the Tupi Monde and the Xavante from Brazil. Soc Sci Med 42: 17351743.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Enrique Teran, Colegio de Ciencias de la Salud, Universidad San Francisco de Quito, Diego de Robles s/n y Pampite, Quito, Ecuador. E-mail: eteran@usfq.edu.ec

Authors' addresses: Edy Quizhpe and Gladys Ñauta, Ministerio de Salud Publica del Ecuador, Quito, Ecuador, E-mails: edyquiz@yahoo.com and glads82@yahoo.com. Juan Antonio Córdoba-Doña, Department of Public Health and Clinical Medicine, Epidemiology and Global Health, Umea University, Umea, Sweden, and Consejeria de Salud, Junta de Andalucia, Cadiz, Spain, E-mail: anecordoba@yahoo.es. Enrique Teran, Colegio de Ciencias de la Salud, Universidad San Francisco de Quito, Quito, Ecuador, E-mail: eteran@usfq.edu.ec.

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