Table 1
The relation between sex and age, level of education and Spanish level.
| Sex | | |
Male n = 40 | Female n = 32 |
Variables | | M ± SD | n | % | M ± SD | n | % | X2 | p |
Age | | 58 ± 18 | | | 57 ± 18 | | | | |
< 30 years (n = 5) | | 3 | 60.0 | | 2 | 40.0 | | |
31–50 (n = 31) | | 15 | 48.4 | | 16 | 51.6 | 1.50 | 0.82 |
51–70 (n = 19) | | 11 | 57.9 | | 8 | 42.1 | | |
71–90 (n = 15) | | 10 | 66.7 | | 5 | 33.3 | | |
> 91 years (n = 2) | | 1 | 50.0 | | 1 | 50.0 | | |
Level of education | Nonliterate (n = 70) | | 38 | 54.3 | | 32 | 45.7 | 1.64 | 0.43 |
Elementary school (n = 2) | | 2 | 100 | | 0 | 0 |
Higher education (n = 1) | | 1 | 100 | | 0 | 0 |
Spanish level | None (n = 46) | | 23 | 50.0 | | 23 | 50.0 | 2.69 | 0.44 |
Beginners (n = 9) | | 6 | 66.6 | | 3 | 33.3 |
Intermediate (n = 4) | | 2 | 50.0 | | 2 | 50.0 |
Advanced (Fluent) (n = 13) | | 9 | 69.2 | | 4 | 30.8 |
From the survey (Table 2), 65% of the participants state that they did not sign or agree with any informed consent when approached. Nearly all (96%) of the participants reported giving at least three blood samples for research, 29% of participants reported feeling pressured to provide samples and 75% of survey participants were given some level of explanation for blood donation. Nevertheless, participants state that 75% of these explanations were in a language other than their native tongue.
Table 2
Opened and closed questions.
Questions | Sex |
Male n = 40 | Female n = 32 |
n | % | n | % |
Q1. Have you had blood samples taken? | Yes | 36 | 52.9 | 32 | 47.1 |
No | 4 | 100.0 | 0 | 0 |
Q2. How many times have you taken blood samples? | None | 3 | 100.0 | 0 | 0 |
1 to 2 | 29 | 52.7 | 26 | 47.3 |
3 to 4 | 3 | 100.0 | 0 | 0 |
> 5 | 1 | 33.3 | 2 | 66.7 |
NA | 4 | 50.0 | 4 | 50.0 |
Q3. Did you receive any kind of pressure or coercion for the extraction of blood samples? | Yes | 11 | 52.4 | 10 | 47.6 |
No | 19 | 57.6 | 14 | 42.4 |
NA | 10 | 55.6 | 8 | 44.4 |
Q4. Did they explain the purpose of this in your language? | Yes | 29 | 53.7 | 25 | 46.3 |
No | 9 | 56.3 | 7 | 43.8 |
NA | 2 | 100.0 | 0 | 0 |
Q4.1. What did you understand of the purpose? | Some diseases | 26 | 59.1 | 18 | 40.9 |
Medical checks | 1 | 50.0 | 1 | 50.0 |
Hepatitis | 3 | 42.9 | 4 | 57.1 |
Paludism | 1 | 33.3 | 2 | 66.7 |
NA | 9 | 56.3 | 7 | 43.7 |
Q5. Did you sign any type of informed consent prior to the extraction? | Yes | 8 | 66.7 | 4 | 33.3 |
No | 26 | 55.3 | 21 | 44.7 |
NA | 6 | 46.2 | 7 | 53.8 |
Q6. Was it national or foreign personnel that approached you for the study? | National | 15 | 62.5 | 9 | 37.5 |
Foreign | 11 | 45.8 | 13 | 54.2 |
Both | 5 | 71.4 | 2 | 28.6 |
NA | 9 | 52.9 | 8 | 47.1 |
Q8. Do you know anyone who has had blood samples taken? | Yes No | 34 0 | 56.7 0.0 | 26 0 | 43.3 0.0 |
NA | 6 | 50.0 | 6 | 50.0 |
Q10. Were there sick people in your community at the time of? | Yes | 1 | 50.0 | 1 | 50.0 |
No | 18 | 56.3 | 14 | 43.8 |
NA | 21 | 55.3 | 17 | 44.7 |
Q11. Did the physicians return to perform some type of treatment related to the samples? | Yes | 0 | 0.0 | 0 | 0.0 |
No | 38 | 55.9 | 30 | 44.1 |
NA | 2 | 50.0 | 2 | 50.0 |
Q12. Did they tell you that the samples were going to be moved out of Ecuador? | Yes | 8 | 61.5 | 5 | 38.5 |
No | 28 | 51.9 | 26 | 48.1 |
NA | 4 | 80.0 | 1 | 20.0 |
Q13. Would you agree that your blood or a product of it is marketed by third parties? | Yes | 0 | 0 | 0 | 0 |
No | 38 | 54.3 | 32 | 45.7 |
NA | 2 | 100.0 | 0 | 0 |
Q14. Do you think your rights were affected in any way? | Yes | 31 | 54.4 | 26 | 45.6 |
No | 0 | 0.0 | 0 | 0.0 |
NA | 9 | 60.0 | 6 | 40.0 |
*NK = Not Know |
Participants recalled that 33% of the staff extracting the blood were foreigners, 56% reported that the medical personnel came from oil companies, and 17% reported being asked to provide samples by missionaries. Only 3% of the participants recalled someone being sick when the blood extraction was conducted. The vast majority (94%) recalled that the scientists or physicians never came back with the results of the samples or any treatments for ailments.
Most participants (75%) were unaware that their blood would be sent abroad for further analysis, and 79% believed their rights were infringed during the experiments. Ninety-seven percent of the subjects rejected the idea their blood could be shared or commercialized in any way, by any institution, in any country.
Interview results
We interviewed 55 out of the 72 participants that were surveyed by our team (response rate 76.4%). The team grouped the coded segments in five categories as follow:
Who was responsible for collecting the sample?
This set of themes referred to the person who led the blood sample collection. The stories included both: national and foreigners medical professionals, missionaries, and colonist related to the oil company. In this category, 46 quotes were identified including some of the following examples, with the responses given in Wao-Terero translated to Spanish, then English:
“The physicians that came to the community were from Ecuador and from other places, they used Dayuma to translate between us.” Case ##03, Age group 71–90 yrs.
“Someone translated, it was the Americans themselves who learned the language at the summer language institute (IVL), so they can study us." Case ##02, Age group 51–70 yrs.
How many times your blood was drawn?
The domain in which the Waorani reported how many times they have given blood has shown that on average, the community members have experienced three blood extractions for research purposes in the last 40 years. This domain was found in 7 occasions and included testimonies like this:
“Our blood was extracted at least two times. The first one around 1984 and a second time in 1991, with help of the missionaries.” Case ##04, Age group 51–70 yrs.
Voluntariness of the extraction
This category referred to freedom in the decision-making process when natives gave their blood. The pressure or coercion arose from the entire community and from the research team. All cases reflect that they never signed any paper giving their consent either for the purpose mentioned or for other studies outside the country. The burden imposed on the tribe to offer the blood had nine quotes, including testimonies like the following:
“We were concentrated in the Teweno Community with more than 100 other Waorani, more than 20 years ago, where we were allocated for the study” Case ##50 Age group 51–70 yrs.
“They told us that the doctors who were going to draw the blood came to our communities to see if we have Hepatitis A, B and C diseases. They took family by family. My daddy did not want to give blood, but the brother said yes, that he should go because it is a very serious illness and he could die” Case ##19, Age group 51–70 yrs.
Communication used during the studies:
This category ranges from the language they used (Spanish or English instead of Wao-Terero) to the understanding of the commands that were given. The analysis of the interviews reflects that in some cases, the team leaders did translate part of the information to be given while in other cases, they did not.
“We were moved in addition to other families towards the community of Teweno. The translator was not happy. We had some trouble with it." Case ##02, Age group 71–90 yrs.
According to the Waorani, the understanding of the purpose for the visits was to see if their blood was good or bad, or to check for diseases in order to perform new treatments. No further information was given on the purpose of the studies.
Returning with the results and final destination of the samples:
This category reflects that researchers told the Waorani they will return to their communities with the results, nevertheless, in very few occasions they did but, in most cases, the Waorani reported they never came back.
“When extracting the blood, they did not give us any information. We were transferred to Teweno, with the help of the missionaries” Case ##06, age unknown, estimated between 80–100 yrs.
The Waorani state they did not know about the future of their blood, nor about the possibility of commercializing it for any economic value.
“I knew they were going to investigate our diseases. Nevertheless, they never told me they were going to take the samples abroad. I did not agree with that, with selling the samples, we are human, I feel hurt, I didn't agree with that” Case ##57, age group 51–75 yrs.
“No, they never came back, once they left, they never came back” Case ##57, age group 71–90 yrs.
Use of samples for research
From our search, thirty-eight studies were identified to have carried out research on the Waorani population. A greater number of studies were carried out by international institutes, mostly by United States of America (USA) (n = 18; 47.4%), followed by European countries (n = 13; 34.2%), countries of Central and South America (n = 6; 15.8%) and Japan (n = 1; 2.6%) (Table 4).
Eighty-nine percent of the published studies used Waorani blood samples 2,844 times between 1978–2016. Twenty-three percent of the studies reported obtaining genetic samples. The majority of the studies (84%) included authors from outside of Ecuador. Seventy-one percent of the studies used samples directly from the population (71%) for research after being collected, and 29% of the samples were obtained from biorepositories. The majority of the studies (68%) did not report obtaining research ethics board approval and 71% did not report obtaining the informed consent of the participants prior to the execution of the project.
Basic research studies aimed to analyze biological samples such as serologic test, skin test data and stool examination. The origin of the samples is classified into two types: primary, those that were obtained directly from the population (n = 22; 71%); and, secondary (n = 9; 29%) that were obtained from gene banks belonging to international institutions such as Coriell Institute, Lawrence Livermore National Laboratory, National Institute of General Medical Sciences or genetic samples obtained from other studies [19–27].
It is evident that the majority of the studies did not mention to get an informed consent of the participants before the commencement of the project (n = 27; 71.0%), neither ethics committee approval national nor international (n = 26; 68.4%)
Table 3 was not provided with this version.
Table 4
Chronological order of publications and details of Waorani’s research.
N° | Institution's country | Author | Year | Number of population | Communities of origin | Study method | Material | Origin of samples | Ethics committee approval | Informed consent |
1 | USA | James W. Larrick et al.[28] | 1978 | 600 Waorani | ND | Observational Epidemiological study | Surveys | - | ND | ND |
2 | USA | Jonathan E. Kaplan et al.[29] | 1980 | 293 Waorani | Tiweno, Tzapino, Gabaro | Basic research, analytical procedures | Serologic test, skin test data and stool examination | Primary | ND | ND |
3 | USA | Jonathan E. Kaplan et al.[30] | 1980 | 227 Waorani | Tiweno, Tzapino, Bai's, Gareno | Basic research, analytical procedures | Serologic test, skin test data and stool examination | Primary | ND | ND |
4 | UK | Theakston RD, et al.[31] | 1981 | 223 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | ND | ND |
5 | USA | James W. Larrick et al.[32] | 1983 | 227 Waorani | ND | Basic research, analytical procedures | Serologic test, skin test data and stool examination | Primary | ND | ND |
6 | USA | E.Wade Davis et al.[33] | 1983 | ND Waorani | ND | Observational Epidemiological study | Descriptive evaluation | - | ND | ND |
7 | UK | Theakston RD et al.[34] | 1983 | 7 Waorani | ND | Applied Basic research - Animal study | Inoculation of human antibodies against the snake venoms | Primary | ND | ND |
8 | USA | James W. Larrick et al.[35] | 1985 | 231 Waorani | Tzapino, Bai's, Tiweno, Gabaro | Basic research, analytical procedures | Serologic test | Primary | ND | ND |
9 | USA | C. Edward Buckley et al.[36] | 1985 | 229 Waorani Other foreign groups | ND | Basic research, analytical procedures | Serologic test and skin test data | Primary | ND | ND |
10 | USA | James W. Larrick et al.[37] | 1987 | 70 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | ND | ND |
11 | USA | David I. Watkins et al.[38] | 1992 | 17 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | ND | ND |
12 | BRASIL | Fabrício R. Santos et al.[39] | 1996 | 1 Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - Coriell Institute of Medical Research | ND | ND |
13 | USA | Evan E. Eichler et al.[20] | 1996 | 1 Waorani | ND | Basic research, analytical procedures | Arrayed X-chromosome library | Secondary - Lawrence Livermore National Laboratory | ND | ND |
14 | GERMANY | Colm O’Huigin et al.[40] | 1997 | 6 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | ND | ND |
15 | BRASIL | Fabrício R. Santos et al.[21] | 1999 | ND Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - National Institute of General Medical Science | ND | ND |
16 | USA | Michael A. Kron et al.[41] | 2000 | 31 Dicaro Waorani 8 Non-Dicaro Waorani 16 Quichua | Dicaro | Basic research, analytical procedures | Serologic test | Primary | ND | Acquired |
17 | ECUADOR | Stephen R. Manock et al.[42] | 2000 | 173 Waorani | 15 Waorani Villages | Basic research, analytical procedures | Serologic test | Primary | Leadership of ONHAE | ND |
18 | BRASIL | Francisco M. Salzano[43] | 2002 | ND Waorani | ND | Systematic review | - | - | Local and National ethics committees | ND |
19 | USA | Lizhi Yu et al.[22] | 2003 | 1 Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - Coriell Institute | ND | ND |
20 | JAPAN | Yasuhiro Go et al.[23] | 2005 | 1 Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - Coriell Institute | ND | ND |
21 | MEXICO | Maria Mercedes Meza et al.[24] | 2005 | 1 Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - Coriell Institute | ND | ND |
22 | USA | Eray Tuzun et al.[25] | 2005 | 1 Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - Coriell Institute Cell Repository | ND | ND |
23 | ESPAÑA | Fabricio Gonzales[44] | 2006 | 40 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | ND | Acquired |
24 | USA | Nicholas J. Marini et al.[26] | 2008 | ND Waorani | ND | Basic research, analytical procedures | DNA sample | Secondary - Coriell Institute Cell Repository | ND | ND |
25 | USA | Stephen Beckerman et al. [45] | 2009 | 121 Waorani | ND | Observational Epidemiological study | Surveys | - | Institutional Review Boards of Pennsylvania State University and the University of Connecticut | Acquired |
26 | ESPAÑA | Fabricio Gonzales et al.[46] | 2009 | 35 Waorani 102 Mestizos 102 Kichwa 102 Afro- Ecuadorian | ND | Basic research, analytical procedures | Serologic test | Primary | Metropolitan Hospital | Acquired |
27 | ESPAÑA | M. Baeta et al.[1] | 2009 | 111 Waorani | Toñampare, Bameno | Basic research, analytical procedures | Saliva swab samples | Primary | ND | ND |
28 | USA | William Kuang-Yao Pan et al.[47] | 2010 | 221 Quichua 99 Shuar 78 Huaorani 50 Cofan 31 Secoya | ND | Observational Epidemiological study | Surveys | - | University of North Carolina at Chapel Hill | ND |
29 | ESPAÑA | Luis Gomez - Perez et al.[48] | 2011 | 36 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | University of the Basque Country | Acquired |
30 | GERMANY | Maria Geppert et al.[49] | 2011 | 65 Waorani | ND | Basic research, analytical procedures | Buccal swab samples | Primary | Approved by an ethical commission not specified | Acquired |
31 | ESPAÑA | S Cardoso et al.[50] | 2012 | 36 Waorani | ND | Basic research, analytical procedures | Serologic test | Primary | Institutional Review Board from UPV/EHU | Acquired |
32 | ESPAÑA | Luis Gomez - Perez et al.[51] | 2013 | 36 Waorani Other foreign group | ND | Basic research, analytical procedures | Serologic test | Primary | Institutional Review Board from UPV/EHU | Acquired |
33 | GERMANY | Lutz Roewer et al.[52] | 2013 | 40 Waorani Fifty different ethnic groups | ND | Basic research, analytical procedures | Buccal swabs, liquid saliva and capillary blood | Primary | Institutional review board of the Institute of Legal Medicine and Forensic Sciences, Berlin | Acquired |
34 | USA | Douglas S.London et al.[53] | 2014 | 16 Waorani 63 Kiwchas | Kawymeno | Basic research, analytical procedures | Stool samples | Primary | ND | ND |
35 | USA | Douglas S.London et al.[54] | 2015 | 121 Waorani 312 Kiwchas | Kawymeno | Observational Epidemiological study | Surveys | - | Institutional Review Board at Arizona State University | Acquired |
36 | UK | Massimo Mezzavilla et al.[55] | 2015 | 22 Waorani 9 Kiwchas | ND | Basic research, analytical procedures | Serologic test | Primary | Institute of Legal Medicine and Forensic Sciences, Germany | Acquired |
37 | GERMANY | Maria Geppert et al.[27] | 2015 | 20 Waorani 24 Kiwcha | ND | Basic research, analytical procedures | DNA sample | Secondary - obtained of other studies | ND | ND |
38 | ECUADOR | Edy Quizhpe et al.[56] | 2016 | 199 Waorani | 22 Waorani Villages | Observational Epidemiological study | Surveys | - | ND | ND |
The table only described the indigenous communities belong to Ecuador. In the origin of the samples: Primary refers to obtaining samples directly from the population and secondary refers to obtaining genetic samples from gene banks belonging to international institutions. ND = Not described. |