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Cigarette smoking and the frequency of colposcopy visits, treatments and re-referral.

Many women attending a city hospital for colposcopy visits are current smokers, so this can be a useful time to highlight the link between cigarette smoking and cervical abnormalities. Identification of a woman as a current smoker presents an opportunity to offer assistance for her to become smoke-free. The aim of this study was to demonstrate the impact cigarette smoking can have on the cervix and the need for cigarette smokers to have more follow-up visits, treatments and re-referrals for colposcopy visits than non-smokers. This research was undertaken as a retrospective descriptive study that compared the persistence and recurrence rates of cervical intraepithelial neoplasia (CIN) with individual smoking status in women who attended the colposcopy clinic. Ethnicity was also examined to discover whether Maori women and other ethnic groups were disproportionately represented at the colposcopy department.


Cervical cancer is the second most common form of cancer in women, worldwide (Bosch, Lorincz, Munoz, Meijer, & Shah, 2002; Sankaranarayanan & Ferlay, 2006) and the eighth most common cancer affecting women in New Zealand (Ministry of Health, 2007a). Cigarette smoking is associated with many cancers, including cervical cancer, and the likelihood of developing cervical cancer is lower in non-smokers and former smokers (Munoz, Castellsague, de Gonzalez, & Gissmann, 2006). While the risk of developing cervical cancer decreases once a woman becomes smoke-free, how long it takes before the risk declines is unclear (Dresler, Leon, Straif, Baan, & Secretan, 2006; ICESCC et al., 2006).

The incidence of cervical cancer in New Zealand women was recorded at 6.9 per 100,000 in 2002 (Ministry of Health, 2006b). This rate was the same as in Australia, and lower than the United Kingdom (8.3 per 100,000). The highest incidence of cervical cancer recorded is in Latin America, with an incidence rate of 33.5 per 100,000. Some of the lowest incidence rates have been recorded in China with a rate of 2.7 per 100,000 (Parkin, 2006) (see Table 1).

Cervical cancer impacts significantly on younger women and is recognised as a serious cause of years of life lost for women in developing countries. For example, in countries such as those of Latin America and Eastern Europe cervical cancer causes more years of life lost than tuberculosis, acquired immune deficiency syndrome (AIDS) and maternal circumstances. Globally it is estimated that cervical cancer is responsible for 2.7 million years of lost life (age-weighted) (Yang, Bray, Parkin, Sellors, & Zhang, 2004). In New Zealand, 200 women are diagnosed annually with invasive cancer of the cervix, and approximately 60 women die each year from the disease (Ministry of Health, 2006b). Cervical cancer is the third most common form of cancer in Maori women in New Zealand, and the fourth leading cause of death for Maori women (Ministry of Health, 2007a).

Tobacco smoking in New Zealand and ethnicity

Tobacco smoking is recognised as the chief cause of preventable death in New Zealand. It is estimated that, on average, 4,700 men and women die each year from smoking-related illnesses (Health Sponsorship Council, 2007). At all ages Maori have the higher rate (47%) of smoking, with Maori women having the highest rate of 50% (Ministry of Health, 2007b). While 27.5% of 15 to 19 year olds were reported to smoke, Maori girls have a 60% smoking prevalence, almost double that of young Maori men (32%). However, this picture is reversed for Pacific teenagers--young Pacific girls' smoking prevalence is 28% compared to young Pacific men (46%) (Ministry of Health, 2006c).

Research Design

This was a quantitative descriptive study, using a stratified random sample. That approach was used as some of the variables in the population were known and their inclusion essential to achieve representativeness.


This study examined records from patients who attended for the first time at the colposcopy clinic between 1 January 2001 and 31 December 2001. Of 1100 women seen in 2001, 500 met the inclusion criteria, and 494 participants were followed-up until 31 December 2006. Patients were included in the study if they met the criteria and excluded if they had any of the conditions outlined in Table 2.


Data regarding how often clients had attended for treatment were collected from treatment registers. All other data were obtained from clients' clinical records. Data available from assessment forms included age, ethnicity, smoking behaviour, LSIL/HSIL diagnosis, combined oral contraceptive pill (COCP) usage, parity, gravida, biopsy, treatment type, number of treatments, treatment type at each follow-up appointment, cancer, genital warts, re-referral, weight and height, and 'did not attend' (DNA) status.

Ethical approval from the University of Otago Board of Studies was granted. Consultation with a Maori Research Office representative took place prior to commencement of the study, and a Maori Research Manager requested that the findings related to Maori women be disseminated appropriately to Maori researchers, health providers and health professionals.

Data analysis

Data were entered onto an Excel spreadsheet by the researcher, and then checked for errors. The checked data was imported into the Statistical Package for Social Sciences (SPSS) version 13. All data variables of interest were found to be normally distributed. Data analysis in this study utilised descriptive and inferential statistics to describe and characterise demographic data. This information is reported as percentages, frequencies, mean, risk ratio, and odds ratio.


Five hundred women were eligible for inclusion in the study, however, six did not attend and were then removed from the study. The remaining 494 women were aged between 20-69 years, with the mean age being 29.83 years (SD. 8.87 years). The participants were 84.6% European, 5.7% Maori, and 0.8% Pacific Island, which reflected the ethnic distribution of the population for the city hospital region.

Smoking behaviour

The smoking status of women attending the colposcopy clinic was routinely collected at each clinic appointment in order to complete the medical history. Smoking status at the time of first clinic visit was therefore known for all 494 women and showed that 44.9% (n=222) women were smoking at the time of data collection. The number of cigarettes smoked per day was identified for 130 women, with 64 smoking less than 10 cigarettes per day. For 92 women, this information was not stated (see Figure 1).

Ethnicity, cervical intraepithelial neoplasia (CIN), and attendance rates

While non-Maori women had a 1.28 greater odds ratio of having CIN, this was not statistically significant (p = 0.65). One of the seven women in the study recorded as having squamous cervical cancer identified as Maori. Maori women were found to be significantly more likely not to attend (DNA) the clinic for colposcopy when compared to non-Maori (OR 3.05, CI 1.41 to 6.63, p = 0.0006).

Smoking and ethnicity

It was found that women with a non-European ethnicity were 1.25 (CI 0.70 to 2.25) times more likely to smoke than European women, although this difference was not statistically significant (p = 0.46). Twenty (71.4%) of the 28 (5.7%) Maori women in the study, reported smoking. Maori women were significantly more than three times likely to report smoking when compared to all other women in the study (OR 3.27, CI 1.41 to 7.57, p = 0.005), although the numbers of Maori women attending the colposcopy clinic were low.

First treatment at colposcopy clinic and smoking status Of the 364 (73.7%) women treated at the colposcopy clinic (two participants took up private care), women who reported smoking, when compared to women who did not smoke were significantly more than twice as likely to need a further treatment as were non-smokers (RR 2.10, CI 1.37 to 3.21, p = 0.001) (see Table 3). In relation to those who reported smoking, 78.4% (n=174 out of 222) had CIN compared to 73.9% (n=201 out of 272) of non-smokers. Therefore, smokers were 1.28 times more likely to have CIN. However this difference was not statistically significant (p = 0.29).

Treatments to remove abnormalities from the cervix were recorded as LLETZ biopsy, cone biopsy, laser treatment, hysterectomy, ablation, private follow-up and no treatment. Among the 494 study participants, 74.1% (n=366) first treatments were carried out, with a LLETZ procedure being the most common and accounting for 43.3% (n=214) of the procedures. Hysterectomies accounted for only 0.2% (n=1) of the procedures, while 0.4% (n=2) of the women had private follow-up. Women who reported smoking were nearly twice as likely to need a second treatment as non-smokers (RR 1.90, CI 0.84 to 4.31). However, the number of study participants needing a second treatment was very low (n = 25), and not statistically significant (p = 0.15).

Follow-up visits and smoking status, ethnicity, age, gravida, parity and COCP

The cohort of 494 was observed in relation to the number of follow-up visits each participant needed and their smoking status. Women who smoked compared to those who did not smoke, were 1.61 times more likely to need a second follow-up appointment, more than three times more likely to need a third and fourth follow-up appointment, and almost three times more likely to need a fifth follow-up appointment than non-smokers. These differences were all statistically significant. Ethnicity, age, gravida, parity and COCP use were not statistically significantly associated with number of follow-ups.

Number of re-referrals

Of the 494 study participants, 91.9% (n=454) required only one referral, although 8.1% (n=40) required a second referral after being previously discharged from the colposcopy clinic. Within the study period, the maximum number of re-referrals for any woman was three, with only four women requiring a third re-referral. Of the 40 women requiring second referral, 25 reported smoking. Smokers were significantly more than twice as likely to need a second referral (RR 2.12, CI 1.12 to 4.23, p = 0.03). Although the numbers were too low to carry out any meaningful analysis, two women needing a third referral reported smoking and two did not. Age, ethnicity, gravida, parity and COCP use were not significantly associated with the need for more than one referral.

The 8.1% (n= 40) of women requiring a second treatment would be considered an acceptable figure (Ministry of Health, 2005; Sellors & Sankaranarayanan, 2003). For this group of women, it was found that while they were nearly twice as likely to be smokers as non-smokers (RR 1.90, CI 0.84 to 4.31), this difference was not statistically significant. However, as numbers were low caution is advised when interpreting these results. The study identified that within the study period 454 of the women required one referral to the colposcopy department. In relation to second referral, 40 (7.3%) required a second referral. For women in this second referral group, it was found that smokers were more than twice as likely to have a second referral as were non-smokers (RR 2.12, CI 1.12 to 4.23). This difference was statistically significant (p = 0.03). In relation to women requiring three referrals, four such women were seen, with two of this group smoking and two not smoking. No analysis was performed on this group as it was too small for the results to be meaningful. Age, ethnicity, gravida, parity and OCP use were not statistically significantly associated with needing more than one referral.

The results demonstrated that for all second, third, fourth and fifth follow-up visits, the women who attended were more likely to be smokers than non-smokers (see Table 3). At the first follow-up there were found to be a 60% (CI 1.11 to 2.34; p = 0.014) likelihood of the woman having been reported as a smoker when she presented as a new patient in 2001. At the third and fourth visits, women who smoked were over three times more likely to attend than women who did not smoke. At follow-up five, the numbers of women needing a colposcopy were 28, with 19/28 of this group reported as smoking (OR 2.74, CI 1.21 to 6.17; p = 0.018). Unlike smoking, other variables such as ethnicity, age, gravida, parity and COCP use were not statistically significantly associated with number of follow-ups.


During the course of this research, a number of limitations that may have impacted on the outcomes were identified. The most significant of these related to the number of years spent smoking and the number of cigarettes smoked. While the smoking status of women was identified in all of the records used in the study, information relating to the length of time smoking and the number of cigarettes smoked could have been helpful when interpreting the results. It would be useful in a future study to have a prospective design and ask further questions related to the intensity and duration of the participant's cigarette smoking habit. In addition, caution needs to be taken with respect to analyses where small numbers were observed, particularly with regard to Maori and Pacific women. During the timeframe of the study, inaccuracies in the recording of ethnicity have been noted therefore the numbers may well be under-counted. Some patients had an initial colposcopy examination but failed to attend follow-up appointments. As a result, the data related to on-going visits in relation to persistence and recurrence of cervical abnormalities is incomplete. It is noted that there is a clear link between socioeconomic status, smoking and cervical abnormalities (Ministry of Health, 2005); however, because of the retrospective design of the study data relating to socioeconomic status was unable to be obtained.


This study has shown that smoking cigarettes can adversely affect the health of the cervix. Women who smoke are at greater risk of requiring more referrals to colposcopy, more follow-up visits and treatments to their cervix than women who do not smoke. The risk of cervical abnormalities for women who become smoke-free is less than for women who continue to smoke; therefore, smoking cessation is potentially beneficial to reduce the need for women to have ongoing follow-up, treatments and referrals, and to reduce the risk of cervical cancer (International Collaboration of Epidemiological Studies of Cervical Cancer et al., 2006; Richardson et al., 2005). While it is widely known in the medical profession that cigarette smoking is a risk factor for squamous cell carcinoma, this link is not so widely known in the general population. Dissemination of this information to women and health professionals could improve the smoking cessation rate and thereby reduce the number of colposcopy interventions required. It also has the benefits for the colposcopy service in terms of reduction of numbers of repeat visits for women.

Maori women in New Zealand are shown to have the highest rate of mortality from cervical cancer, followed closely by Pacific women (Sadler et al., 2004). Maori and Pacific Island women were identified as being three times more likely to not attend appointments than non-Maori women. This highlights the need to consider alternative means of improving ongoing attendance for colposcopy. This is an area requiring further research.

Previous research has identified that many women, regardless of their smoking status, may come into contact with the Human Papillioma Virus (HPV), but at some point in the disease process cigarette smoking either encourages acquisition of the HPV or assists in the disease progressing to CIN (International Collaboration of Epidemiological Studies of Cervical Cancer et al., 2006; 2005; Munoz et al., 2006). In studies undertaken throughout 22 countries HPV DNA has been found in 99.7% of all cervical cancers (Clifford, Franceschi, Diaz, Munoz, & Villa, 2006). The current study provides further support for this trend. However, although women who presented with CIN were 1.28 times more likely to smoke when compared to non-smokers, this difference was not statistically significant. (p = 0.29). McIntyre-Seltman, Castle, Guido, Schiffman, and Wheeler's (2005) study of 5,060 women found the development of HPV was only weakly associated with cigarette smoking; but that the progression of HPV to CIN III was greater in women who smoked compared to women who did not smoke (OR 1.7; 95%; CI 1.4 to 2.1).

Although smoking is associated with an increased risk of squamous cell carcinoma (Koushik & Franco, 2006; Richardson et al., 2005; Vaccarella et al., 2008) it is still unclear whether smoking increases the risk of developing, or the persistence of, HPV. Two recent studies further support the present study. In these it was found that women who smoked had an increased incidence of HPV, and women with a greater smoking intensity were more likely to have HPV (Richardson et al., 2005; Vaccarella et al., 2008). The two large studies previously identified, where women who develop CIN and cervical cancer were found to be more likely to be smokers (International Collaboration of Epidemiological Studies of Cervical Cancer et al., 2006; McIntyre-Seltman et al., 2005; Munoz et al., 2006), also support the findings of this research.

While women who have had a treatment for CIN have been identified as being at an increased risk of developing further CIN (Cestero, 2006; Kalliala, Anttila, Pukkala, & Nieminen, 2005), the risk that women who smoke will require a second treatment is greater than that for women who do not smoke (Acladious et al., 2002). This study found that women who smoked were more than twice as likely to need further treatment when compared to women who did not smoke. In a United Kingdom study, the risk of treatment failure was found to be 3.17 times higher for women who smoked than that for non-smokers. (Acladious et al., 2002). This same study also took account of the intensity and duration of smoking and confirmed that the greater the number of cigarettes smoked, the greater the tendency for treatment failure (Acladious et al., 2002).

The two studies previously discussed (Acladious et al., 2002; Vaccarella et al., 2008) support the research reported here in that they demonstrated that women who smoke are more likely to have persistence and recurrence of HPV, LSIL and HSIL. It is expected that women who experience persistent and recurrent HPV and CIN will require more interventions, which may include additional examinations, diagnosis, and treatments to remove cervical abnormalities. A number of the other studies examined also support these findings, showing that women who smoke are at a greater risk of developing CIN III or SCC than are non-smoking women (Gunnell et al., 2006; International Collaboration of Epidemiological Studies of Cervical Cancer et al., 2006; McIntyre-Seltman et al., 2005). While the Ministry of Health (2006a) found that in 2001 approximately 23% of the Canterbury female population was smoking, in the present study for the population of women attending the colposcopy clinic that figure was about doubled (44.9%).


The results show conclusively that cigarette smoking increases the likelihood of women requiring further colposcopy visits, treatments and re-referrals. The results identified that when compared to non-smokers, women who smoked were three times more likely to need a third follow-up visit, and twice as likely to need further treatments to remove abnormalities. Women who smoked were also twice more likely to require a second referral than women who did not smoke. The link between smoking and the frequency of colposcopy visits, treatment and re-referrals supports the need for intervention to encourage smoking cessation. This need is particularly the case for Maori and Pacific women as they are more likely to smoke than those of other ethnic identities.

Both the research results and the literature indicate the importance of linking colposcopy interventions and promotion of smoke-free behaviour. The literature has also indicated that the link between smoking and CIN needs wider and stronger dissemination to health professionals, women, and their families. Girls reaching puberty should also be targeted with the information that cigarette smoking is associated with damage to the cervix, and that the risk of HSIL and cervical cancer is greater for those starting smoking at a young age (International Collaboration of Epidemiological Studies of Cervical Cancer et al., 2006; Tolstrup et al., 2006).


Acladious, N. N., Sutton, C., Mandal, D., Hopkins, R., Zaklama, M., & Kitchener, H. (2002). Persistent human papillomavirus infection and smoking increase risk of failure of treatment of Cervical Intraepithelial Neoplasia (CIN). International Journal of Cancer, 98(3), 435-439. doi: 10.1002/ijc.10080

Bosch, F. X., Lorincz, A., Munoz, N., Meijer, C. J., & Shah, K. V. (2002). The causal relation between human papillomavirus and cervical cancer [Electronic Version]. Journal of Clinical Pathology, 55, 244-265. Retrieved from

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Dresler, C. M., Leon, M. E., Straif, K., Baan, R., & Secretan, B. (2006). Reversal of risk upon quitting smoking. The Lancet, 368, 348-349. doi:10.1016/S0140-6736(06)69086-7

Gunnell, A. S., Tran, T. N., Torrang, A., Dickman, P. W., Sparen, P., Palmgren, J., & Ylitalo, N. (2006). Synergy between cigarette smoking and human papillomavirus type 16 in cervical cancer in situ development. Cancer Epidemiology, Biomarkers & Prevention, 15, 2141-2147. doi:10.1158/1055-9965.EPI-06-0399

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McIntyre-Seltman, K., Castle, P. E., Guido, R., Schiffman, M., & Wheeler, C. M. (2005). Smoking is a risk factor for cervical intraepithelial neoplasia grade 3 among oncogenic human papillomavirus DNA-positive women with equivocal or mildly abnormal cytology. Cancer Epidemiology, Biomarkers & Prevention, 14, 1165-1170. doi:10.1158/1055-9965.EPI-04-0918

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J. Lamb RN, BN, MHSc, Clinical Nurse Specialist, Colposcopy Department, Christchurch Women's Hospital, Christchurch, NZ.

S.I. Dawson RN, BSC (Hons), MSc and Public Health Research, PhD, Senior Manager, Population Health Manager, BAML, Perth, Australia.

M.J. Gagan PhD, PHCNP, FAANP, CEO, Nurse Practitioners First Ltd. Christchurch, NZ.

D. Peddie FRANZCOG, MRCOG, Consultant Gynaecologist & Obstetrician, Christchurch Women's Hospital, Christchurch, NZ.
Table 1.
Incidence of Cervical Cancer in 2002

Country           Rate per

China             2.7
New Zealand       6.9
Australia         6.9
Canada            7.7
United States     7.7
Sweden            8.2
United Kingdom    8.3
Latin America     33.5

Note: Sourced from Munoz et al. (2006);
New Zealand Ministry of Health (2006b);
Wain, (2006).

Table 2.
Inclusion and Exclusion Criteria

Inclusion Criteria         Exclusion Criteria

* New patient              * Under 20 years of age or
* No previous colposcopy     over 70 years of age
* Presented at the         * Previous presentation to
  colposcopy department      the clinic for colposcopy
  in 2001                    prior to referral during
* Age 20 years of age        2001.
  to 69 inclusive          * Previous colposcopy
* Had low grade            * Treatment to occur at a
  intraepithelial            different facility
  lesions (LSIL) or high   * Glandular abnormality
  grade intraepithelial    * Vulval abnormalities that
  lesions (HSIL) on          may or may not include
  their cervix.              the cervix

Table 3.
Smoking Status and Number of Follow-up Appointments

              Smokers    Non-smokers    RR         CI          p
              (n=222)      (n=272)
              (Rate %)    (Rate %)

Follow-up 1     100%        100%        --         --          --
Follow-up 2     92%          83%       1.61   1.11 to 2.34   0.014
Follow-up 3     58%          27%       3.21   1.95 to 5.28   <0.001
Follow-up 4     37%          15%       3.43   1.83 to 6.43   <0.001
Follow-up 5     19%          9%        2.74   1.21 to 6.17   0.018

Figure 1. Smoking Status

Number of cigarettes
smoked per day

<10            64

10 to 20       43

20 to 30       21

30 to 40        2

Not Stated     92

Quit During     3

Never         269

Note: Table made from bar graph.
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Author:Lamb, J.; Dawson, S.I.; Gagan, M.J.; Peddie, D.
Publication:Nursing Praxis in New Zealand
Article Type:Report
Geographic Code:8NEWZ
Date:Mar 1, 2013
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