Setting and governance

We conducted a cross-sectional questionnaire study between October 2013 and March 2014 in Hull and Leeds in the Yorkshire and the Humber region (YH). Hull had the highest smoking prevalence (26.4%) in YH (YH prevalence = 20.1%) in 2014, which was also much higher than the national prevalence (18.0%) according to the Integrated Household Survey (IHS) [22]. The prevalence in Leeds was also higher than national prevalence and the fourth highest in YH (23.1%). Ethical approval was received from the NHS YH-Leeds East Research Ethics Committee (Reference: 12/YH/0341).

Participants

Data collection

The questionnaire development was informed by the: Model of Pathways to Treatment [26], Cancer Awareness Measure (CAM) [27] and Symptoms Appraisal questionnaire [25]. The questionnaire comprised sections on the experience of symptoms of lung and head and neck cancers, pre-existing illnesses/conditions, response to symptoms, triggers to consultation, understanding/awareness of potential cancer symptoms, symptoms interpretation, health services utilization and socio-demographic data (S1 Questionnaire). ‘Cancer’ was not mentioned in the participant information sheet (PIS) or questionnaire. It was only mentioned in the section that explored the respondents’ understanding of potential cancer symptoms, which included cancer as one of the four illnesses (others were ‘flu’, heart disease and asthma). After piloting, patients over fifty years (smokers and practice-matched non-smokers) from GP lists in Hull and Leeds were sent a postal questionnaire (with one reminder). We regarded receiving a completed questionnaire from a respondent as consent to participate in the study.

Measurements

Analysis

Baseline characteristics were produced for broad demographic indicators, smoking status, ‘having cancer experience’ and ‘having a previous cardiorespiratory diagnosis’. We examined differences in the socio-demographic characteristics by smoking status. The proportions of symptoms experienced, self-reported consulting and awareness of potential cancer symptoms were also examined. The strength of association between smoking status and: symptoms experienced; self-reported consulting; and awareness, for cough, breathlessness, tiredness and shoulder pain was assessed (Chi-squared test). Logistic regression was used to investigate the relationship between smoking status and awareness of, experience of and self-reported consultation for cough, breathlessness, tiredness and shoulder pain. Adjustment for demographic characteristics (age, gender, education and accommodation), previous cancer experience and cardiorespiratory diagnosis was made in the models. Analyses focused on these symptoms as they were most commonly reported by our study population and in previous research [32]. Cough, breathlessness and tiredness are among the six key symptoms included in the National Institute for Health and Care Excellence (NICE) guidelines for suspected lung cancer [33]. Additionally, cough and breathlessness are part of the national cancer awareness campaigns in England [34]. We regarded missing data as missing-completely-at-random (MCAR) [35]. Data were analyzed using STATA 14.

Sample characteristics

The study population comprised 1205 respondents; 45.5% men and 53.1% women (Table 1), mean age 62.8 years (SD = 8.8; range = 50–98), mostly White British (97.2%). Just over half of the sample had never smoked (53.6%), with 25.8% smokers and 18.3% ex-smokers. The final sample comprised more ex-smokers than expected. Among ex-smokers, 71% had stopped smoking over 12 months prior the study, while 28% had stopped smoking within the previous 12 months. The average number of cigarettes smoked per day by 306 respondents was 12.7 (SD = 7.6, range 0–40); 26.4% were classed as heavy smokers, the proportions of moderate and light smokers were the same (36.8%). There was no evidence of an association between smoking status and age (p = 0.062), gender (p = 0.297) or ‘having a previous cardiorespiratory diagnosis’ (p = 0.473). However, there was evidence of a relationship between smoking and education (p = 0.034), accommodation (p<0.001) and cancer experience (p = 0.003).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 1. Sample characteristics, frequencies and association with smoking.

https://doi.org/10.1371/journal.pone.0183647.t001

Cough

Almost a fifth of our respondents (19.2%) reported experiencing cough; of these, less than half had consulted their doctor (36.0%) (Table 2), but 60.1% of all respondents were aware that cough is a potential cancer symptom. Experience of cough was associated with smoking status (p<0.001), with experience being more common amongst smokers than never-smokers (adjusted OR = 2.56 95% CI[1.75–3.75]). Amongst the smokers (34.2%) who experienced cough, only about a quarter consulted for this (24.4%)(Table 2). Smoking status was related to consulting for cough (p = 0.011) with smokers less likely to consult than never-smokers (adjusted OR = 0.37 95%CI[0.17–0.80]) (Table 3). There was no evidence of an association between smoking and awareness that cough could be a cancer symptom (p = 0.898).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 2. Frequencies for symptoms experience, self-reported consulting and awareness of cough, breathlessness, tiredness and shoulder pain and the association with smoking status.

https://doi.org/10.1371/journal.pone.0183647.t002

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 3. Univariate and multivariate logistic regression findings for the association between smoking status and reporting, consulting and awareness of cough, breathlessness, tiredness and shoulder pain.

https://doi.org/10.1371/journal.pone.0183647.t003

Breathlessness

Just over a tenth of the respondents (10.9%) reported experiencing breathlessness. A third of those experiencing the symptom consulted (33.0%) but only about a quarter (25.6%) were aware that breathlessness is a potential cancer symptom (Table 2). Experience of breathlessness was associated with smoking status (p = 0.002) and was more common amongst smokers than never-smokers (adjusted OR = 2.39 95% CI[1.43–4.00]). Over a fifth of smokers were aware that breathlessness is a potential cancer symptom (23.3%). Smoking status was associated with awareness that breathlessness was a potential cancer symptom (p = 0.035) with ex-smokers more likely to be aware than never-smokers (adjusted OR = 1.65 95% CI [1.12–2.41]) (Table 3). There was no evidence of an association between smoking and consulting for breathlessness (p = 0.304).

Tiredness

Less than half of our respondents (40.9%) reported experiencing tiredness; of these, about a fifth consulted their doctor (20.1%) (Table 2) and 39.4% of all respondents were aware that tiredness is a potential cancer symptom. Smoking status was associated with experience of tiredness (p = 0.004) with tiredness being more common amongst smokers than never-smokers (OR = 1.57 95% CI [1.12–2.19]). There was no evidence of an association between smoking and consulting for tiredness (p = 0.818) or awareness of tiredness as a potential cancer symptom (p = 0.125).

Shoulder pain

Just over a tenth of our respondents (13.9%) reported experiencing shoulder pain. Of these, less than half had consulted (35.4%) (Table 2), but about a fifth (21.1%) of all respondents were aware that shoulder pain is a potential cancer symptom. There was no evidence of an association between smoking and experiencing shoulder pain (p = 0.081); smoking and consulting (p = 0.125) or smoking and awareness of shoulder pain as a potential cancer symptom (p = 0.933) (Table 3).

Main findings

Smoking was associated with increased experience of cough, breathlessness and tiredness. Smokers were more likely than never-smokers to experience the three symptoms while ex-smokers were more likely than never-smokers to experience breathlessness and tiredness. Smoking status was associated with consulting for cough but not for the other three symptoms. Smokers were less likely to consult for cough than never-smokers. Smoking status was associated with awareness for breathlessness as a potential cancer symptom but not with the other three symptoms. Ex-smokers were more likely than never-smokers to be aware of breathlessness as a potential cancer symptom while smokers were just as aware of breathlessness as never-smokers.

Comparison with other studies and possible explanations for our findings

Being a current smoker was associated with increased experience of cough, breathlessness and tiredness, which are among the six key symptoms associated with suspected lung cancer [33]. It was also associated with consulting for cough as confirmed by Friedemann Smith et al [19] Previous evidence has suggested that generally cough is not recognized as a potential cancer symptom hence the time taken to present to the doctor with cough is longer [6]. This is especially the case for smokers, who usually have a ‘smoker’s cough’ and so will normalize cough [9]. This may lead to consulting their doctor later than average [13]. Other evidence suggested that smokers were less likely than never-smokers to use preventive/cancer screening services [37]. There was no association of smoking status with consulting for the other three symptoms probably because there is generally low awareness of potential cancer symptoms [8].

Previous research suggested that breathlessness rarely occurred in isolation and that it normally occurred in combination with other symptoms associated with lung cancer [23]. This therefore highlights the importance of focusing on the multiple symptoms of lung cancer [32,33], particularly in public health media campaigns.

Strengths and limitations

This is the first study to focus on experience of-, consulting and awareness of symptoms suggestive of lung and/or head and neck cancer in relation to smoking status. Previous research has mainly focused on a single area such as prevalence [24], awareness [7,18,21], or consulting [13,22]. There is limited evidence combining these three areas. Most evidence relating to cancer focuses on lung cancer [16,17], with less evidence on head and neck cancers [14,15].

Ours is also the first study to focus on experience of-, consulting and awareness of symptoms suggestive of lung and/or head and neck cancers among smokers over 50 years, a group at high risk of several cancers, and to sample in such a way as to obtain a reasonable return from smokers. We obtained a similar response rate to similar postal questionnaire studies [38,39]. We also achieved the proposed sample size probably because our recruitment areas had higher than average smoking prevalence than the YH and English figures [22]. Our findings for symptoms experienced and consulting were empirical unlike the awareness findings, which were not empirical findings, but reflected the respondents’ health literacy. We were therefore able to obtain estimates of symptoms experienced and consulting within our study population. Cough, breathlessness, tiredness and shoulder pain are common and are among the key symptoms for suspected lung cancer in the NICE guidelines [33] therefore these findings are clinically relevant. We did not mention ‘cancer’ in the PIS and questionnaire; we referred to the questionnaire as the ‘Symptoms Awareness Study’ to reduce the risk of biased responses from our respondents. This was done so as to reduce/prevent the respondents’ over-reporting that they consulted for a given symptom if the study had been about ‘cancer’. This way we were more likely to obtain the respondents’ true consulting behaviour.

Smoking status was self-reported, which may be a valid marker for assessing tobacco exposure [40]. However, when considering the self-reported never-smokers caution should be taken since there might be the possibility of misclassification because of stigma whereby, the ‘never-smoker’ might have lied about their smoking status. To avoid this, biochemical tests, which are more accurate, are recommended [40]. This was a postal questionnaire which suggests that people with low literacy skills may have been excluded. The study respondents were mostly White British with very limited ethnic minority involvement suggesting that these findings cannot be generalized to a multicultural community and may instead be relevant to a similar population. We do not have information on the number of ethnic minority individuals who were invited to participate in the study; therefore we do not know whether there was a non-response bias among the ethnic minority groups. The response rate was low although within the parameters of questionnaire studies [38,39], thereby suggesting the possibility of bias in the study sample. Although our criterion for recruitment was ‘no cancer diagnosis’, few respondents were diagnosed with cancer; to minimize this effect on cancer awareness, we controlled for ‘cancer experience’ in adjusted analyses. Additionally, since these symptoms are also present in other non-cancer diseases (cardiorespiratory conditions) and could influence our consulting findings, we controlled for ‘having previous cardiorespiratory diagnosis’.

Implication

Our findings highlight the importance of targeting not only smokers but ex-smokers as they also reported experiencing breathlessness and tiredness, some of the key symptoms associated with lung cancer [33]. Our findings also suggest that cancer awareness interventions should focus on the key potential cancer symptoms rather than a singular symptom [23,32,33]. Drawing on the consulting findings, innovative interventions targeting smokers, particularly those with cough symptoms, to improve their consulting behavior should be considered. In order to understand this population’s low consulting behavior, further work on the attributions of potential cancer symptoms in older people should be considered.