Every year, millions of patients are diagnosed with pulmonary nodules, and as increasing numbers of people undergo lung cancer screening, even more patients will be found to have a nodule. The vast majority of patients cannot benefit from the detection of a pulmonary nodule because most are benign. Accordingly, it is important to develop strategies to minimize harm, in particular the distress of a “near-cancer” diagnosis. In other settings, communication strategies are critical mediators of patient-centered outcomes for those with cancer and those at-risk of cancer. We conducted multiple studies to characterize the experience of patients with the diagnosis and evaluation of incidental pulmonary nodules, measure patient-centered outcomes for patients with pulmonary nodules, and determine the association of patient-clinician communication practices with those outcomes. We learned that a substantial proportion of patients experience distress and inadequate communication about pulmonary nodules and their evaluation, and yet many clinicians are unaware of the degree to which some patients are affected by the finding of a pulmonary nodule. The present review provides a comprehensive summary of our results and offers suggestions for how clinicians can best provide high-quality communication for their patients.
Key Words: health communication, lung cancer, pulmonary nodule
Abbreviations: CPS, Control Preferences Scale; PCP, primary care provider; VA, Department of Veterans Affairs
Every year, millions of patients have an incidental pulmonary nodule identified on chest imaging studies,1, 2 and the number of nodules will only increase with implementation of lung cancer screening.3 Although the vast majority of nodules are ultimately determined to be false-positive findings for lung cancer,4, 5 it is challenging to determine if a small nodule is malignant when first identified. Expert guidelines recommend active surveillance, often managed by nonspecialists, to detect the few cases of lung cancer at an early stage when cure rates are substantially better.6, 7
Although few stand to benefit, all patients are at risk of iatrogenic harm from detection and evaluation of a pulmonary nodule. Accordingly, it is important to mitigate the severity and frequency of these harms. Harris et al8 proposed a taxonomy of harms that result from a “near-cancer” diagnosis after a nodule is detected through lung cancer screening. This taxonomy applies equally to incidental nodule detection and includes physical harms, psychological harms, financial strain, and opportunity costs.
We believe it is critical to evaluate patient-centered outcomes following nodule detection for several reasons. First, incidental nodule detection is already common, and with the advent of screening, clinicians risk becoming inundated with patients with pulmonary nodules that require evaluation. Second, we wanted to evaluate patients with a low risk of lung cancer because this group represents the vast majority of those with a nodule. Many studies have focused on the impact of cancer detection on patients but fewer on the impact of a “near-cancer” diagnosis.
Third, almost everyone with a nodule has a risk of suffering psychological harm. When we started our research studies, however, there were no data on the likelihood or magnitude of those harms. As an example from a related setting, we knew that patients with false-positive mammograms frequently experience distress.9, 10 In the context of false-positive mammograms, distress is often short-lived and resolved when results of a breast biopsy are negative. However, most patients with pulmonary nodules undergo radiographic surveillance rather than biopsy, leaving them in a state of uncertainty for months or years about whether they have cancer. We each had clinical experiences talking with patients who experienced profound and prolonged distress after their pulmonary nodule was detected. Thus, we wanted to study how commonly distress occurred and how severe it was for patients with nodules. We focused on psychological harm because most patients with small nodules undergo radiologic surveillance and are less likely to suffer physical harm or financial strain. Furthermore, for the subset of patients who do undergo invasive procedures, physical harms may be hard to change, as they result from mostly fixed patient and imaging characteristics (eg, comorbid illness, size and location of nodule).
Finally, and most importantly, we wanted to understand if there were mechanisms to influence distress and other patient-centered outcomes. We hypothesized that communication strategies would be a likely, if not the only, mechanism to influence distress. We also reasoned that understanding this communication process would provide valuable insights into how clinicians made recommendations about nodule surveillance and what impact these processes had on patients’ adherence to recommendations.
The Studies BeginSimultaneously but independently, we applied for and were awarded career development awards from the National Cancer Institute (Dr Wiener) and the Department of Veterans Affairs (VA) (Dr Slatore). The proposed studies were a mix of qualitative and quantitative analyses of patients with nodules along with the clinicians who care for these patients. The main differences in the designs were that Dr Wiener included patients from several health-care systems in the northeastern United States and focused on large-scale cross-sectional analyses. Dr Slatore performed a smaller study but with longitudinal evaluations and only included patients from one VA facility in the northwestern United States. The goal of the studies was to evaluate the association of communication practices, as reported by both patients and clinicians, with patient-centered outcomes. The primary outcome was distress, but adherence, knowledge, and satisfaction were also studied. When available, validated instruments were used to measure these outcomes (Table 1).
Table 1.Associations of Communication Domains With Patient-Centered Outcomes
Measure/Exposure Outcome Direction (If Exposure Increasing) General quality of communication Distress Decreased (baseline and longitudinal)21, 22 Perceived lung cancer risk No association21 Adherence (patient) Improved27 Adherence (clinician) No association27 Information exchange Satisfied with information Distress No association21 Perceived lung cancer risk No association21 Perceived lung cancer risk Distress No association (in baseline and multicenter)21, 19 Adherence (patient) No association27 Adherence (clinician) No association27 Actual risk No association19 Inability to estimate risk Distress No association21 Mode (letter vs other); clinician role Distress No association21 Patient as person Partnership with the clinician Distress All decreased22 Relationship with the clinician Positive approach Interest in participant’s life Decision-making Preferred role Distress No association22 Actual role Distress No association22 Satisfaction with care No association37 Quality of medical care No association37 Perceived lung cancer risk No association37 Nodule information satisfaction No association37 Concordant with actual decision and preferred role in decision-making Distress No association22 Satisfaction with care Improved37 Quality of medical care Improved37 Perceived lung cancer risk Not associated37 Nodule information satisfaction Not associated37 Other notable associations Objective risks of lung cancer (eg, age, smoking status, nodule size, Mayo calculated risk) Distress No association21a Perceived risk of lung cancer Increased22 Posttraumatic stress disorder Distress Increased21 Perceived risk of lung cancer Decreased21 Depression Distress Increased19, 21 Distress Adherence (patient) Decreased27 Adherence (clinician) No association27We were guided by theoretical models of patient-centered communication to help measure and analyze communication strategies. These models emphasize the separate practices that comprise communication, which can each be measured and replicated. Most models agree on four core domains (Fig 1): (1) information exchange, in which a clinician informs a patient about the risks and benefits of diagnostic and treatment options; (2) understanding the patient as a person and his or her preferences and values, which can be divided into tasks such as fostering healing relationships, responding to emotions, and managing uncertainty11; (3) shared decision-making, which combines adequate information exchange with considering patients’ values and preferences to make an informed decision that is shared between the patient and clinician; and (4) establishing a therapeutic alliance so that the patient and clinician are “on the same page.” Some patient-centered communication models also emphasize the “clinician as person” domain, which incorporates the personal qualities of the clinician. This domain was used to guide qualitative interviews of clinicians about their practices and communication surrounding nodule evaluation. As recommended by the National Institutes of Health and the American Thoracic Society,12, 13, 14 we sought to understand the longitudinal association between communication and distress to better assess the causal nature of this relationship.
Figure 1.The figure shows a theoretical model of the possible relationships between different domains of patient-centered care and patient-centered outcomes among patients with incidentally detected pulmonary nodules.
Based on the patient-centered communication model,15, 16 our primary hypothesis was that high-quality communication would be associated with less distress. We further hypothesized that high-quality communication in the information exchange domain, measured by a patient’s self-perceived risk of lung cancer, was the most important mediator of distress for patients with nodules. Our experience was that many patients overestimated their risk of lung cancer, and these patients seemed to be more distressed than those who recognized their cancer risk to be low. Finally, we hypothesized that shared decision-making would be strongly associated with knowledge about the nodule because a core tenet of shared decision-making is providing the necessary medical information about risks, benefits, and options.
What We FoundOverall, most of our results from both cohorts studied were similar and complemented each other, with a few differences that are highlighted here.
As we suspected, many participants were distressed after they were diagnosed with an incidental nodule. Our qualitative studies showed that many seemed not at all or only mildly distressed, but some reported severe levels of distress, particularly in the period immediately following nodule detection. For example, one participant reported how she “bawled through Christmas”17 while another reported feeling like he had received a “death sentence”18 after finding out about the nodule. Many of our participants reported that they immediately assumed they had cancer (Table 2).17 Our quantitative results confirmed these findings. For example, in Dr Wiener’s cross-sectional study19 among patients with an average nodule size of 7 mm (median risk of lung cancer according to the Mayo20 model was 7.1% [interquartile range, 4.6%-10.3%]), who were surveyed up to 3 years after the nodule was detected, 50% reported at least mild distress (measured with the Impact of Event Scale), with 24% experiencing moderate or severe levels.19 In Dr Slatore’s longitudinal study of patients with an average nodule size of 6 mm (average risk of lung cancer, 10% [SD, 12%]) who were surveyed, on average, 4 months following detection, 39% reported distress, 16% at moderate or severe levels.21 Although the average levels of distress decreased over time, almost 60% reported having mild or greater levels of distress at least once during surveillance, and 25% still had at least mild distress after 2 years of nodule surveillance.22 Notably, the average distress scores in both our studies were higher than those reported among lung cancer screening trial23, 24 participants with nodules, although they followed the same trend of a short-term peak in distress that tended to decline over time.25, 26
Table 2.Representative Quotes
Outcome Patient Perspective Physician Perspective Distress My kidney doctor calls me up and says, “Oh by the way, we found a tumor on your lungs.” They didn’t even know what it was, but it was just the way [he] came out and said it. I was devastated.… I bawled through Christmas.17We also evaluated adherence to recommendations regarding nodule surveillance, including the separate contributions of patients and clinicians in the chain of adherence. We found in our longitudinal nodule study that patients and clinicians were each adherent approximately 75% of the time, and almost 40% of participants had at least one episode of nonadherence during surveillance,27 echoing the results of other studies.28, 29, 30 Importantly, clinician nonadherence was not associated with lung cancer risk factors, suggesting that when clinicians deviate from surveillance guidelines, they make this decision based on factors extrinsic to the patient’s objective risk of lung cancer, a result found in other studies.29, 31 However, despite reporting in qualitative studies that clinicians sometimes deviate from guidelines (eg, order an earlier scan) based on a patient’s distress (Table 2),32, 33 there was no association between distress and clinician adherence. This finding suggests that clinicians underestimate distress or do not guide management decisions based on it. Furthermore, some clinicians believed there was an “optimal” level of distress that might motivate patients to be more adherent to recommended surveillance and that completely alleviating distress might have the unintended consequence of reducing adherence.32 In actuality, however, patients who were distressed were less adherent to surveillance, and there was no level of distress that was associated with improved adherence. This finding is similar to results in other cancer screening settings,34 in which distress surrounding a false-positive result is negatively associated with adherence to subsequent screening. By contrast, high-quality patient-clinician communication (as rated by patients) was associated with increased patient adherence to recommended nodule surveillance.
These results quantified the occurrence and magnitude of the problems, but we wanted to evaluate how communication strategies might mitigate them. In general, participants were satisfied with communication with their clinicians overall, and many reported it to be of high quality. However, we also found some systemic problems. Focusing first on the information exchange domain in our qualitative studies, we learned that participants had very little information about their nodules, a sentiment voiced by virtually every participant in our studies. Indeed, we titled our first papers, “What do you mean, a spot?”17 and “What the heck is a nodule?”18 because those were the exact words so many used when describing their experiences. The participants implicitly understood that the nodule was related to lung cancer, but very few had an accurate understanding of the level of risk, the plans for surveillance, or the rationale for active surveillance rather than biopsy (Table 2).
These findings were confirmed in our quantitative studies,19, 21 in which most participants dramatically overestimated their risk of lung cancer. For example, in the longitudinal study, the mean ± SD lung cancer risk was 10% ± 12%,20 whereas the average perceived risk was 39% ± 26%. Cancer risk was < 30% for 95% of participants, but only 30% perceived that the risk was < 30%. Participants also knew very little about the natural history of pulmonary nodules,19 and their knowledge did not improve over the course of surveillance.22, 35 The large majority of participants reported that they did not receive or could not remember receiving information about their risk of cancer.19
Because patient self-report only reflects one-half of the communication dyad, we also interviewed primary care providers (PCPs) and pulmonologists to learn their approach to communication with patients with pulmonary nodules. PCPs confirmed that they seldom directly provided information about the risk of lung cancer (Table 2) and other details about surveillance to their patients.32 They offered several explanations, including lack of time, lack of confidence in their own estimate of cancer risk, and the concern that providing too many details would be overwhelming and might actually increase patient distress. Pulmonologists, who mostly described seeing patients with larger nodules, more often provided risk information, although not universally.33 Thus, we are confident that most patients with small nodules receive little information about their nodule, and the information they do receive is seldom tailored to their individual cancer risk.
Interestingly, and contrary to our hypotheses, self-perceived risk of lung cancer, as a measure of adequate information exchange, was not consistently associated with distress. Although distress was common, it was not nearly as frequent as patients’ near universal lack of knowledge about cancer risk. Despite their limited knowledge of cancer risk, many patients were satisfied with the care and information they had received and did not seem distressed. This dichotomy seemed to be explained by the patients’ trust in their clinicians, which was related to how clinicians communicated in the patient as person domain (Table 2). As one participant said, “She’s a good doctor, because she would call me back if it was serious. She wouldn’t just let me go.”18
We also evaluated the association between information exchange and distress quantitatively. Perceived risk was not associated with distress in the large cross-sectional study or at baseline in the longitudinal study. However, perceived risk was modestly associated with distress in the longitudinal analyses, even though distress levels decreased during the period of active surveillance while perceived risk remained stable (a trend confirmed by the qualitative analyses). Overall, these findings suggest that strategies designed to improve knowledge about small nodules, with a goal to align the actual and perceived risk of lung cancer, may be insufficient to mitigate distress.
We next evaluated the association between the patient as person domain and distress. The qualitative studies suggested that patients experienced less distress when their clinicians were empathic and generated trust (Table 2).17, 18, 26 The quantitative studies strongly confirmed this finding. In the longitudinal study, we evaluated specific aspects of the patient as person domain and found that communication strategies which included partnership with the clinician, a personal relationship with the clinician, whether the clinician provided a positive and a clear approach to the problem, and whether the clinician was interested in the participant’s life were all associated with decreased distress.22
Turning to shared decision-making, we asked if participants wanted to make decisions by themselves about nodule surveillance, whether they wanted their clinician to decide for them, or whether they wanted to share the decision. In the quantitative studies, using the Control Preferences Scale (CPS),36 participants almost always had a preferred role for the surveillance decision (56% shared, 24% clinician-controlled, and 20% patient-controlled) but in almost 40% of encounters, they could not describe their actual role.37 Although most patients wanted to participate in decision-making,19, 37 patients infrequently engaged in decision-making with clinicians,38 often not recognizing that a decision had even been made. This finding was corroborated by clinicians who also reported that they seldom provided the level of information about the nodule that would be required to engage in true shared decision-making. In an international survey of clinicians who care for patients with pulmonary nodules, one-half reported that they are open to shared decision-making with patients about nodule evaluation.39 In qualitative interviews, however, PCPs and many pulmonologists reported that they rarely engaged in shared decision-making with their patients about nodule evaluation (Table 2).32, 33 Based on these findings and the fact that information exchange about nodules was often inadequate, we suspect that true shared decision-making about nodule surveillance options seldom occurs, despite guidelines for pulmonary nodule evaluation explicitly recommending shared decision-making.7
Among those participants able to rate their role in decision-making, a shared process was not associated with satisfaction with or perceived quality of medical care, lung cancer risk, reported quality of information received, or distress.22, 37 However, role concordance in decision-making (ie, having the same preferred and actual decision-making roles) was associated with satisfaction with and perceived quality of medical care, although not with knowledge or distress. Similarly, the inability to report how the decision was made was not associated with distress (G. C. S., unpublished data).
Finally, the therapeutic alliance domain of communication was qualitatively evaluated. Not surprisingly, given the inadequate knowledge about nodules, patients often did not know the plan for surveillance (Table 2).17, 18, 19, 35 This lack of therapeutic alliance may explain some of the failure of distress to diminish over time among some patients. Most patients did not understand that surveillance is typically limited to 2 years (depending on nodule size) or that radiographic stability over that interval usually confirms that the nodule is benign.17, 19, 26 Without that understanding, some patients experienced persistently elevated levels of distress throughout the period of radiographic surveillance and even after surveillance had ended.22, 26 Meanwhile, the lack of therapeutic alliance and consequent poor understanding of the evaluation plan may also explain our finding that patients often were nonadherent to the surveillance plan. Without a robust nodule-tracking system in place, some patients would have failed to receive any surveillance at all.27 Unfortunately, systems to prevent patients from “falling through the cracks” during nodule evaluation are not available in many health-care settings,40 despite being recognized as a critical need by clinicians.32
Summary and RecommendationsThese studies confirmed our hypotheses that for patients with incidentally detected nodules, distress is common, sometimes severe, and often long-lasting. A parallel finding is that nonadherence to recommended surveillance is frequent, with multiple causes. In general, patients were satisfied with the communication with their clinicians in the patient as person domain and often reported high levels of trust. However, there were clear deficiencies in patients’ knowledge about nodules and a lack of shared decision-making. Despite these communication deficiencies, their impact on distress and adherence may be low. Indeed, it seems that communication strategies focusing on the patient as person domain are more likely to have an effect on patient-centered outcomes.
Clinicians were worried that too much distress was obviously detrimental to patients. They used multiple strategies to decrease distress but one that stood out was some clinicians’ decision to avoid talking about cancer. Patients uniformly asked for more information about nodules, specifically about the risk of cancer, and those who did receive it more often found this information reassuring rather than anxiety-provoking.19 Accordingly, the strategy of withholding cancer information to reduce distress is likely ineffectual. Clinicians also believed that no distress might be associated with worse adherence. Our results echo those from mammography,34 which also found that distress is associated with worse adherence with no “optimal” level. Thus, we believe that the risk of unintended consequences from interventions designed to increase knowledge about the risk of lung cancer and/or decrease distress is low.
The link between actual risk of lung cancer, perceived risk, and distress is both interesting and complicated. We hypothesized that a large driver of distress for patients with nodules would be a misperception that the risk of lung cancer was much higher than the actual risk. Although we found that indeed this misperception was common, it does not seem to be strongly associated with distress. Interventions that focus on information about nodules, one of the primary goals of decision aids, may be necessary to improve knowledge but are likely not sufficient to improve distress if used on their own without communication strategies that also include communication about individual patient’s values and preferences.
Despite widespread recommendations for shared decision-making, we were not surprised that it rarely occurred, as in many other clinical contexts.41 Even among participants who could rate how the nodule surveillance decision was made, shared decision-making and role concordance were not associated with distress. We measured shared decision-making with the CPS, a widely used but imperfect instrument.42, 43 Our findings on the whole indicate that “true” shared decision-making, with adequate information exchange and consideration of patients’ preferences and values, seldom occurred. The CPS does not capture these subtleties, and we therefore suggest not using the CPS as a single measure of successful shared decision-making. It may be adequate to use in preliminary studies of new communication interventions, such as decision aids, as a measure of communication processes but may not be appropriate as a measure of actual patient-centered outcomes.
Patient and Clinician SuggestionsTable 3 includes several examples of suggestions that participants offered for how clinicians could improve communication. Overall, patients wanted more information about the relative size of the nodule, the associated risk of lung cancer, and the plan for follow-up (e-Appendix 1 includes a sample information letter). Additional strategies that patients found reassuring but were underutilized by clinicians included explaining that nodules were a common finding and highlighting the small size of the nodule on the CT image.19 We also included several examples of how to improve communication in the patient as person domain. Changes in this domain may be challenging but likely essential for improving patient-centered outcomes. Meanwhile, clinicians expressed a need for better tools to share information with patients and systems-level methods to improve adherence to their recommended surveillance. To meet some of these needs, we developed a patient education document about pulmonary nodules.44
Table 3.Suggestions to Improve Patient-Clinician Communication Regarding Pulmonary Nodules
Patient as person Recognize that identifying a pulmonary nodule is often distressful although frequently underreported Discuss the nodule directly with the patient and provide a written summarySchedule an office or telephone visit to discuss the nodule
A written summary should:
Provide information about the nodule and address common concerns
Avoid medical jargon or sending the CT report without further explanation
See
e-Appendix 1for an example of a patient-centered notification letter
“It’s common to be distressed after learning you have a pulmonary nodule; how are you feeling?”
“What’s on your mind?”
“Some people with a nodule worry they have lung cancer… what have you been thinking?”
Provide telephone number for nurse coordinator/manager
Clarify ability to message clinician through the electronic health record
Nodule risk calculator: http://reference.medscape.com/calculator/solitary-pulmonary-nodule-risk
Nodule patient education: http://www.thoracic.org/patients/patient-resources/resources/lung-nodules-online.pdf
“Let’s talk together about what to do about your nodule”
“When we make this decision about what to do about your nodule, some patients want to make the decision on their own, some just want me to decide, and many want something in the middle. How about you?”
“Some people are worried about getting lung cancer when thinking about nodule follow-up; what do you think?”
“I know you have worried about radiation exposure in the past, so let’s talk about that before we decide on a plan.”
“Most of the time, the right decision is to watch the nodule over time, when we get another CT scan. But some people want to have an answer right away. How do you feel about waiting?”
“How would you like to get the results of your next CT scan?”
“To make sure I didn’t forget to tell you anything, can you repeat back to me when you’re going to get your next CT scan? And what are you going to do if you have more questions or start to feel distressed?”
As with all studies, the present studies have limitations. First, the longitudinal analyses and mixed-methods analyses improve the likelihood that the associations observed are causal, but observational studies can never truly assess causality. Thus, communication interventions should be empirically tested for their effect on patient-centered outcomes. Second, because two diverse cohorts were studied, the overall results may be more generalizable than the results would be if taken separately. However, there is still a need to study associations of communication with patient-centered outcomes in other settings, most notably among patients undergoing lung cancer screening. Third, our studies assessed communication as reported by patients and clinicians, which may differ from actual communication. Only recorded or observed studies of clinic visits or telephone conversations can assess what really happened.
ConclusionsMany patients are diagnosed with a pulmonary nodule, and it is common to be distressed, sometimes severely, as a result. Patients want more information and should be provided with it. It is unclear, however, if improved information exchange, by itself and without attention to individual patient values and preferences, will improve patient-centered outcomes. Similarly, shared decision-making is important, but additional or new measures are needed because current instruments are mostly associated with process measures that may be less relevant for patients. Furthermore, decision aids, which mainly focus on knowledge, may not suffice for improving other patient-centered outcomes such as distress.45
Although we focused on patients with incidentally detected nodules, these results from routine clinical practice may be more generalizable to patients with screening-detected nodules in the real world than results from randomized trials.46 If so, screening is likely to cause distress for many patients, and current recommendations to use decision aids may be insufficient to mitigate that distress. We are currently conducting a study to assess the impact of screening and quality of communication on patient-centered outcomes in the usual-care context.47 Given the large number of patients who may undergo screening in the near future, it is important to continue to study and refine strategies to minimize its harm.
AcknowledgmentsFinancial/nonfinancial disclosures: None declared.
Role of sponsors: The sponsor had no role in the design of the study, the collection and analysis of the data, or the preparation of the manuscript.
Other contributions: We are indebted to many people and organizations. First, we thank VA's Health Services Research and Development Service and the National Cancer Institute for sponsoring our studies and career development. We thank our research coordinators, including Terri Kneeland, MPH, Emilie Zoltick, MPH, ScD, Denise Clarke, MBA, Ashley Wagner, MS, and especially Sara Golden, MPH, for doing the lion’s share of the work on these studies. We thank all our mentors for teaching us how to do research and fostering our careers. In particular, we thank David Au, MD, and Michael Gould, MD, for introducing us and showing us that collaboration is way more fun and fruitful than competition. Finally, and most importantly, we thank the study participants. We started and continue this work because of these patients, for the ultimate goal of using our research to make their lives better. The views expressed in this article are those of the authors and do not necessarily represent the views of the Department of Veterans Affairs or the US Government. The Department of Veterans Affairs did not have a role in the conduct of the study; in the collection, management, analysis, or interpretation of data; or in the preparation of the manuscript.
Additional information: The e-Appendix can be found in the Supplemental Materials section of the online article.
FootnotesFUNDING/SUPPORT: This study was sponsored by a Department of Veterans Affairs Health Services Research and Development Service Career Development Award [Grant CDA 09-025 & CDP 11-227] to Dr Slatore and a career development award from the National Cancer Institute [Grant K07 CA138772] to Dr Wiener. It was also supported by resources from the VA Portland Health Care System and the Edith Nourse Rogers Memorial VA Hospital.
Supplementary Datae-Appendix 1
ReferencesThis section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materialse-Appendix 1
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