Abstract
Stomach cancer is the third leading cause of cancer death globally. Helicobacter pylori plays a role in the healthy human gut, but is also associated with multiple chronic diseases, including stomach cancer. Though H. pylori prevalence is declining in parts of the world, it remains high among certain populations. In Arizona, stomach cancer rates are 3–4 times higher among the Navajo Nation population as compared to the non-Hispanic white population. This pilot project assessed adult Diné (Navajo) individuals’ understanding and awareness regarding H. pylori infection and stomach cancer. Focus groups were held in three Diné communities. Data were analyzed thematically using a multi-investigator consensus approach. Participants had limited knowledge of H. pylori infection and stomach cancer, and perceived local medical providers as also having limited knowledge on these conditions. Participants described poor health care experiences, structural inequalities, and environmental concerns, and associated these with H. pylori infection and stomach cancer. This study highlights the need for additional research and education on current knowledge and perceptions of stomach cancer and H. pylori infections in Navajo Nation.
Keywords: Indigenous health, focus groups, qualitative research, gastric cancer, Helicobacter pylori
INTRODUCTION
Helicobacter pylori (H. pylori) is a bacterial infection, which can usually be treated by an antibiotic regimen [1]. The pathogen seems to play a role in healthy human digestion as a component of the microbiome but is also associated with development of duodenal or stomach ulcers, stomach cancer, and stomach mucosa associated lymphoid-tissue (MALT) lymphomas. H. pylori infection and its relationship to cancer mortality and morbidity are not fully understood. Yet, 78% of all stomach cancer cases, and 89% of non-cardia cases, are attributed to chronic H. pylori infection [2].
Recent studies indicate that H. pylori prevalence is declining in developed countries, including those undergoing rapid socioeconomic transition [3–5]. Yet in the United States (US), there are highly elevated annual age-adjusted rates of hospitalization for stomach cancer among American Indian/Alaska Natives (AI/AN) [6]. Furthermore, AI/AN stomach cancer rates vary by geographic regions, Alaska having the highest rates found [7]. For the Diné (Navajo) Nation, a sovereign Indigenous nation in the southwestern US, stomach cancer rates are 3 to 4 times higher compared to the non-Hispanic white population in Arizona [8]. The Navajo Epidemiology Center recently reported the age-adjusted incidence rate of gastric cancer among members of the Navajo Nation to be 14.2 per 100,000, which is nearly four times higher than among the non-Hispanic white population in Arizona [8].
To better understand the factors contributing to the gastric cancer disparity for Diné, focus groups (FG) were conducted in three Navajo communities in the southwestern portion of the Navajo Nation with the goal of assessing adult Diné individuals’ understanding and awareness regarding H. pylori infection and stomach cancer. The average population size of these communities is approximately 1,400 people [9]. Nearly a quarter (23.5%) of Navajo households in Arizona earn less than $10,000 in household income and benefits, with median household income estimated at $26,401 [10]. Community members often travel roughly 30 to 90 minutes by vehicle to nearby Arizona border towns, Winslow and Flagstaff, for necessities, healthcare, entertainment, and other services. The FGs were conducted with the intent of informing strategies to improve the health status of Diné adults diagnosed with H. pylori infection, including gastric cancer prevention, diagnosis, and treatment.
METHODS
A pilot qualitative study was conducted with three Navajo chapter communities regarding their knowledge of stomach cancer and H. pylori risk factors, transmission, diagnosis, treatment, and prevention; attitudes regarding perception of risk for stomach cancer; and practices related to prevention. This entailed the team presenting at the three community chapter meetings to provide information, address any concerns, and discuss possible study approvals and any future recruitment plans. The project successfully attained formal support resolutions from the chapters and their respective Agency Council, a regional governing body comprising chapter groupings. These resolutions are required for study approval by the Navajo Nation Human Research Review Board (NNHRRB)—which was granted. The University of Arizona Institutional Review Board also approved the study in September 2016.
Participant Recruitment.
Participant criteria included: self-identify as a Diné citizen, 18 years and older, and current residency within one of the three chapters’ boundaries. Recruitment fliers were posted on community news boards in each chapter a few weeks before the scheduled FG. On the day of each FG, a large recruitment flyer was posted outside the community Chapter House where the FG was held. In some cases, there were not enough participants to conduct a FG so team members recruited in nearby stores and housing areas.
Procedures.
The all Diné FG team included two co-facilitators and three notetakers, each with varying degrees of Diné K’éhji (Diné language) fluency. Team members were attentive to Diné-centered and kinship-rooted social practices and ensured the FG environment reflected culturally appropriate norms. For instance, the team regarded attendees as socio-cultural (kin) relatives by customarily shaking hands upon arrival, welcoming them with food and beverages, and providing time prior to the FG to establish kinship relations and reconnect with others. The lead facilitator, a man fully fluent in Diné K’éhji, had worked over 30 years for the Navajo Nation government in the fields of social services, workforce development, and youth programming. The woman co-facilitator was a public health researcher employed by a state university. Notetakers consisted of a doctoral student in cancer biology and man, along with two women, one an undergraduate public health student and the other with a hospitality management background.
Facilitators initiated the informed consent process by customarily introducing themselves and detailing their kinship clans in Diné K’éhji, so participants and team members could properly address one another with the appropriate kinship term, which informs on how to respectfully interact. Participants had the option of giving informed consent on their own or as part of a group process. Participants who read through the form on their own were encouraged to pose any questions to the facilitators before deciding to participate. In the group process, the lead facilitator read the informed consent form aloud for the group, answered participants’ questions in English and Diné K’éhji, and explained if individuals chose to participate, they could sign the form to indicate informed consent. The form also asked if the participant permitted to be audio-recorded during the FG discussion. All participants voluntarily consented and all granted permission to be audio-recorded. No one declined to participate. Each participant received a copy of the consent form with signatures from the participant, the project lead, and the NNHRRB chairperson. In February 2017, data collection occurred through 3 FGs that were conducted in English and Diné K’éhji. The facilitators guided FG discussion by asking nine open-ended questions (see Table 1) while notetakers took hand-written notes. Key words identified by the participants during the FG were written on a flipchart for those needing terms spelled out or discussed after the FG. Additionally, the notetaker with a background in cancer biology interjected scientifically accurate information about human anatomy and H. pylori throughout the FGs via drawings on a white board. Importantly, this learning-moment education helped participants better comprehend the questions and address any evolving concerns. FGs ranged from 75 to 102 minutes in length. At the end of each FG, participants received a $20 cash incentive, educational materials about H. pylori and were referred to the Winslow Indian Health Care Center if they had lingering concerns, as investigators have an ethical responsibility to address any concerns that participants may have arisen from focused discussion to minimize harm.
Table 1.
Open-ended questions in focus groups
| Component | Question |
|---|---|
| Stomach cancer | How much of a problem do you think stomach cancer is in the Navajo Nation? |
| Can you list some of the risk factors for stomach cancer? | |
| What do you think are some symptoms of stomach cancer? | |
| What do you think increases the risk of a person’s likelihood for developing stomach cancer? | |
| Helicobacter pylori | Have you ever heard of the bacteria Helicobacter pylori or H. pylori?
|
| Related stomach conditions | What do you know about stomach ulcers?
|
What do you know about chronic gastritis?
| |
| Prevention | What do you think people can do to reduce their likelihood of developing any of the health outcomes we just discussed? |
| Health priorities | Of the topics we talked about today, which do you think was the most important and why? |
Data Analysis.
The data analysis team consisted of the FG co-facilitators, Diné professors in public health and sociology, and undergraduate public health students (one Diné and one Latina). FG audio recordings were transcribed by the lead author and an undergraduate student, with assistance from the fourth author to translate conversations in Diné K’éhji to English. The analysis team used the multi-investigator consensus method because of its strength as a culturally appropriate approach to assess Indigenous-provided data by incorporating the lived experiences and knowledge of individual Diné investigators on the team [11]. This method has been used previously to identify patterns and themes in open-ended responses from Diné participants in a project evaluating a culturally relevant breast cancer education video [12].
Each investigator independently read the transcripts to identify codes (recurring words, concepts and ideas) prior to meeting together in-person for a multi-day analysis session in March and April 2017. As a group, investigators reviewed each question and corresponding participant responses, discussing initial thoughts and codes. Each individually wrote their codes on sticky notes and affixed these to a white board where investigators collectively organized and moved codes into groupings with similar content that indicated patterns. The collective reviewed the emergent patterns together and by consensus identified themes, operationalized here as overarching words that identify a topic or category describing the patterns. Patterns and themes were decided by group consensus, meaning no one individual had the ultimate say in any decision and everyone had an equal voice. Before finalizing any decision, investigators would ask everyone if they agreed with the group decision, ensuring it was acceptable to proceed further. If someone did not agree with a decision, the group would listen to the points of disagreement and then determine how to modify the decision so group consensus was achieved.
RESULTS
A total of 31 adults participated in the three FGs – 12,9 and 10 adults respectively – comprised of 18 women and 13 men (N=31), ranging in age from 22 to 87 years. The first, second, and third FG consisted of 12, 9, and 10 participants, respectively. The first FG occurred in the smallest community (Chapter A) where most participants recruited were those who were already at the chapter house pertaining to other matters. Chapter A is situated between the other two communities (Chapters B and C). Traveling distance between Chapters B and C is approximately 40 miles, and information travels quickly via word-of-mouth. Participants in the last two FGs said they heard about them from other community members.
Focus Group Results
The FGs revealed four saturated themes on: 1) Fear of an unknown disease; 2) Frustration and concern with medical providers and health care services; 3) Structural inequalities compromise quality of life; and 4) Returning to Hózho (Balance) requires resources for communities. See Table 2 for categorization of the themes and subthemes.
Table 2.
Themes identified from focus groups conducted with three Navajo Nation communities
| Themes | Sub-Themes |
|---|---|
| Fear of an unknown disease | • Lack of H. pylori and stomach cancer information • Perceived lack of awareness among medical providers about H. pylori infections • Perceived vulnerability to H. pylori and stomach cancer • Increased anxiety deriving from lack of information • Uncertainty in health diagnosis and information received |
| Frustration and concern with medical providers and health care services | • Feelings of frustration and anger • Negative experiences with medical providers • Incomplete health communication by providers • Passive acceptance of poor healthcare treatment |
| Structural inequalities compromise quality of life | • Drivers of behavioral and nutritional choices • Environmental contamination • Challenges of accessing safe drinking water |
| Returning to Hózhó (balance) requires resources for communities | • Demand for increased community-targeted and driven education • Outreach strategies • Communication channels • Holistic health worldview |
Fear of an unknown disease
Most participants expressed not having any personal or family member’s experiences with stomach cancer, with a few stating the FG was the first time they had ever heard about it. Consequently, participants could not confidently identify risk factors or symptoms of stomach cancer. These discussions often led participants to collaboratively speculate what the symptoms of stomach cancer could be, listing generalized descriptions of “stomach problems” such as bloating, burning of the esophagus, stomach pain, and ulcers. In general, some participants alluded that most people they knew downplayed the severity of stomach symptoms by stating almost dismissively, “It’s just a stomach problem,” or “It’s just a stomachache.” One participant revealed, “I don’t really know anyone who has had stomach cancer so I really wouldn’t be able to tell you because there’s not a whole lot of information about it so I wouldn’t be able to say what could increase [risk].”
Participants suspected they did not receive comprehensive information about stomach cancer at health care facilities because providers likewise had limited knowledge about stomach cancer themselves; thus, providers were not informing community members about risk factors and progressive symptomatology. As one participant explained about the patient-provider interaction, “People are usually told they have ulcer [sic], but never get fully informed of the possibilities of getting stomach cancer.” Another participant commented, “They just examine you and tell you that you’re like this, but they don’t tell you that whole thing. You know, for instance, ‘This has progressed, and now it’s over here, and if it gets to that stage, it’s going to get really dangerous.’ They just say you’re at this one point and then they give you medicine for it. They don’t give you the entire picture.” Discussants wanted a fuller picture of the progression of stomach cancer from the initial infection of H. pylori to cancer, and not being given a point-in-time, disconnected snapshot of infection or cancer.
Further complicating this issue are cultural beliefs that discourage discussions of death, which were thought by some as a partial explanation for the diminished awareness of stomach cancer among Navajo people. As one person stated, “You know when people pass on? They don’t say why they pass on, maybe [stomach cancer] is why they died. Even the person who lived with the person who passed on, they don’t say anything about it.”
All but two participants stated they had never heard of Helicobacter pylori or H. pylori. One woman in her 30s said she knew about it because she had a previous infection which took health providers six months to diagnose. Her esophagus burned so much at one point she recalled that she could not talk. She recalls, “It took them a long time to diagnose. I kept going back, I kept going back. I could tell something was wrong with my body, you know. Something’s not right! But they [health providers] were...they didn’t know how to treat it or what to look for. So it went undetected for a while. Finally, they had me blow into a bag or something. Somebody had that genius idea about this H. pylori.”
Uncertainty surfaced in two ways among a few participants regarding the interconnections between H. pylori and stomach cancer. The first, as just mentioned, involved participants who discussed having direct or family experiences with H. pylori or stomach cancer and recounted themselves or their family members physically and intuitively feeling something was amiss with their stomach or body. When medical visits revealed no answers, they dealt with prolonged states of confusion and anxiety. Second, there was expressed uncertainty about information received about stomach disorders. One participant said her physician advised her not to consume iodized salt because it would damage the stomach membrane as it should only to be used for cleaning harvested animal meat and organs. On ulcers, another said, “I know a couple of people that they get a chili seed stuck in their throat or somewhere, and that chili seed will burn a hole through the lining of the stomach, and they get ulcers from it because…like I’ve known 3 or 4 people that has happened to. And that’s the only thing I’ve really known about ulcers…that it happened from having a chili seed stuck in your system.”
Some participants reported feeling increasing vulnerability to H. pylori infection and stomach cancer risks as discussion progressed. Regarding stomach cancer, one participant exclaimed, “We’re afraid of it,” explaining that all the generated discussion was the reason it was now a prominent health concern for him – to which others uttered or motioned in agreement. Another person said he had only heard of H. pylori once through a conversation but did not think it was serious enough to consider learning more. He remarked, “Since hearing this today, it’s kind of just worrying me a little…like the food I eat and the water I drink. So, I’m just listening…trying to find out more.”
Frustration and concern with medical providers and health care services
Several personal stories of experiences with medical providers were shared, many fraught with anger and frustration toward health care quality and provider communication. Several participants noted nurses were frequently more attentive than physicians to patient needs. A participant shared her family’s experience trying to get adequate medical care for their in-law’s digestive problem, “I lost my brother in-law recently. He said, he’s been vomiting a lot. Every time he eats something, he vomits, and the doctor couldn’t find out what the problem is. [The physician sic] just kept saying, “Naw [sic], nothing’s wrong with him.” They keep saying go home, and finally they…one of my daughter-in-laws kinda [sic] got mad at the doctor, saying, “Examine him!” Then they finally find out what cause…was the cancer in there.”
Some were especially critical of medical providers’ failure to provide patients with resources to manage their health conditions or reduce risk of disease. A participant noted, “You know the [Indian Health Service sic], they don’t inform you with that information. They don’t tell you this is the diet you need to go on. They don’t! They just draw the line right there and they tell you you’re affected with this. They don’t go further.”
A few participants described emotionally draining situations in which they felt like they did not receive proper medical care within reasonable amounts of time. These experiences often led to their feeling resigned to receiving poor healthcare. Others shared instances in which they made multiple and often futile trips to local health facilities because they did not get conclusive explanations for their discomfort, pain, or sense of imbalance. One participant discussed how he had to endure excessive appointment wait times at a local health facility, and then ultimately went to an urban healthcare facility to get the care he needed.
Structural inequalities compromise quality of life
Many participants identified environmental contamination as a potential risk factor for stomach cancer, and listed various examples of contaminants existing near their residence or where livestock were kept, including: coal combustion and mining, pesticides, air quality, and polluted rain run-off from creosote-treated railroad ties. In particular, the discussants expressed concerns with contamination from nearby abandoned uranium mining sites proximal to their water sources for household and agricultural use. One elder thought water delivery pipes were a source of drinking water contamination, explaining that old, rusty pipes delivered to households reddish-colored water that people still used unfiltered for cooking and drinking. Participants also talked about not being adequately informed by water monitoring agencies about the status of their water quality, “Maybe there’s something, some kind of chemical that’s making it dangerous and they’re not letting us know about those type of things.”
Participants also discussed how their community’s behavioral and nutritional choices were constrained by low socioeconomic status and cultural eating habits deemed unhealthy. A participant shared, “The healthy foods are expensive, so we have to go for mutton,” to which fellow participants expressed general agreement. Community members, similar to the general Diné population, said mutton or lamb is readily available for purchase at flea market and roadside food stands or can be freshly butchered if the family has sheep, but is known to be a fatty protein source. A participant concluded for the group, “We like to eat fat mutton.” Later in the discussion, a participant noted, “I think we need to change our lifestyle too. Change which ones [sic] is best for you. Just can’t live on eating fat mutton [laughter].” Another participant talked about how certain necessities are not widely available at community retailers and even if they were available, are considered expensive, “Yeah, like the basic necessities. Like, you have to travel so far to get it and like a lot of the [Native Nation sic] don’t really have money to do that all the time.”
Many homes on the reservation lack refrigeration, which dictates what foods families buy, store, and prepare. A participant noted, “Yeah, I think a lot of people out here on the rez [reservation sic] don’t have refrigeration so, you have to plan accordingly or whatever you bring back that day you have to cook that day. Or eat a lot of canned foods, because you can’t really keep anything. Making it a lot easier for those people without refrigeration that puts them in a higher risk group…from not having their food prepared properly or not stored properly.”
Participants shared their safe water sources as too far to travel by vehicle, and families with limited travel funds were more likely to access closer water sources, such as wells or windmill tanks that may not be designated for human consumption. As one participant explained, “Finances has a lot to do with it. ‘I don’t want to have to pay for the water. I want to just get it for free.’ It’s like that,” reciting what she heard other community members convey.
Returning to Hózhó (balance) requires resources for communities
Participants discussed solutions to improve community health. At the individual level, participants spoke about the importance of taking care of one’s physical, mental, and spiritual wellbeing by making healthy food choices such as eating home-grown foods and decreasing intake of sodium and sugar, practicing spirituality and self-care, exercising, and not being too hard on oneself for past negative behaviors. One participant advised community members to become more cognizant of how local food vendors may or may not be utilizing safe food handling practices.
Participants voiced a strong desire for more education, awareness, and resources on H. pylori, stomach cancer, and related gastric disorders. They suggested informational posters be posted in frequently visited areas like local chapter houses, convenience stores, churches, and community Facebook. Information should also be shared via Diné radio stations and community forums. Several participants emphasized health education topics presented holistically and not fragmented, alluding to Western educational methods that break topics down into pieces. Participants preferred to be informed about the entire process and relationships, “Yes, all of it. This bacterial information process cannot be piecemeal. It has to be the whole thing at once. If we talk about the entirety of it, everybody will get it. They have to cover the whole process. That way people will get the whole idea of what steps and stages it goes to.”
DISCUSSION
Results from FGs conducted within three Diné communities highlighted the need for additional research and education on current knowledge and perceptions of stomach cancer and the H. pylori infection. Furthermore, there is limited knowledge and awareness of the relationship between H. pylori infection and stomach cancer, except for the few individuals who had experienced H. pylori infection or stomach ulcers personally or had heard about related experiences from family and friends. Participants expressed their desire for more community-driven education on the topic, which has shown to be impactful in other studies [13–15].
A common element this study shares with other research from minority communities concerns poor communication between healthcare providers and their patients, treatment delays, and low confidence in healthcare providers [16–18]. Participants expressed growing fears and vulnerability toward H. pylori infection and stomach cancer due to the generalized lack of knowledge and experience amongst the discussants, as well as cultural beliefs regarding restricting discourse surrounding death. Furthermore, these feelings also seemed to derive from a lack of confidence in medical providers’ knowledge, as well as their ability to quickly and accurately diagnose and/or adequately address stomach-related illnesses. A few participants shared their experiences with delayed detection of ulcers or other gastric disorders by medical providers, as well as their frustration and anger about the treatment they suffered. As a result, we recommend the medical provider community provide trainings for healthcare staff members to increase provider knowledge of H. pylori infection symptomology as a way to improve response-time to patients who may potentially have an active infection.
Importantly, participants identified the connection between health and low socio-economic status pointing to the reality of food deserts in their communities, with limited fresh food options and higher costs associated with healthy food. They also discussed the lack of refrigeration as a potential compromise to their wellbeing and the problems encountered in accessing safe drinking water including expenses incurred for families needing to drive farther distances to clean drinking water sources. Participants were forced to decide between higher financial and time costs for safe drinking water compared to the convenience of hauling well water from dubious or unregulated sources. Establishment of additional water hauling stations to reduce traveling costs and health risks could increase access to regulated drinking water [19].
Further, participants were concerned with issues of environmental racism evident within their communities [20]. Specifically, these involve environmental quality and protection along with the potential link with increased risk of H. pylori infection. Participants discussed the need to strengthen environmental protection measures and policies as a way to improve the health and wellbeing of their community [21–22]. Diné tribal governmental, public health and environmental agencies, as well as their partnering agencies at the county, state, and federal levels could explore opportunities for increased coordination to cleanup, prevent, and mitigate environmental contaminants [23]. These coordination efforts should include collaborative input from Diné non-governmental grassroots organizations working at the forefront of local and international Indigenous environmental advocacy efforts [24].
Finally, consistent with Diné beliefs regarding actively striving to return to Hózhó, participants expressed the importance of attending to their physical, mental, and spiritual well-being through healthy food choices, engaging their spirituality, and practicing self-care. Given the almost total lack of information known regarding H. pylori and its relationship to stomach cancer, participants voiced strong appeal for additional resources. They likewise contributed suggestions for effective distribution and consumption to the Diné community. Crucially, this process includes a holistic approach wherein vital information is not reduced into small fragments. To the Diné worldview this prototypical Western fragmented approach obfuscates their comprehension of H. pylori infection [25].
Strengths and Limitations
This is one of the few studies focused on the knowledge and perceptions of H. pylori and stomach cancer in an Indigenous community and, as such, lays the groundwork for future work addressing the issues of stomach cancer in Indigenous populations. However, one potential limitation is that the three communities surveyed were clustered close together, within a 41-mile, or a 45-minute, drive from the first community to the third community. These findings may not apply to other American Indian nations or communities in the Southwest.
ACKNOWLEDGEMENTS
This research was funded by a Cancer Disparities seed grant from the University of Arizona, Arizona Cancer Center (PI: Eyal Oren). Guidance of the research design, implementation, and analysis was also funded by the National Institute of Health (NIH), National Institute on Minority Health and Health Disparities of the National Institutes of Health under Award Number P20MD006872 (Co-PI: Priscilla R. Sanderson, Ph.D., CRC and Nicolette I. Teufel-Shone). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank the participating tribal governmental entities for their support and review of this work. We also thank the university students who worked with the project (Alexis McKinley, Kim Trujillo, and Chelsie Hadley).
Footnotes
Publisher's Disclaimer: This Author Accepted Manuscript is a PDF file of a an unedited peer-reviewed manuscript that has been accepted for publication but has not been copyedited or corrected. The official version of record that is published in the journal is kept up to date and so may therefore differ from this version.
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