The follow-up of patients with head and neck cancer: an analysis of 1,039 patients

HEAD AND NECK

The follow-up of patients with head and neck cancer:an analysis of 1,039 patients

P. Kothari • A. Trinidade • R. J. D. Hewitt •

A. Singh • P. O’Flynn

Received: 10 May 2010 / Accepted: 6 December 2010 / Published online: 31 December 2010

� Springer-Verlag 2010

Abstract In all cancer specialities, there has been much

debate about the best follow-up regime. The provision of

a service that meets high standards whilst being cost-

effective is increasingly pertinent. The objectives of the

study were to examine: whether routine follow-up facili-

tates early diagnosis and recurrence; whether there is a

cohort of patients who require a more intensive follow-up

regime; whether follow-up should be customised to indi-

vidual patients. A total of 1,039 consecutive outpatient

consultations were prospectively analysed in a multicentre

study. All adult patients who had undergone multidisci-

plinary, multimodality management for head and neck

cancer were included. The case mix was representative of

all head and neck tumour sites and stages. Suspicion of

recurrence was noted in 10% (n = 96/951) of patients seen

routinely. This rose to 68% (n = 60/88) for the subset of

patients who had requested an appointment. Most recur-

rences were found within the first follow-up year (n = 64/

156, 54%). Only 0.3% (n = 3/1,039) of asymptomatic

patients attending routine appointments were suspected of

having a recurrence, and two (0.2%) were found to have an

actual recurrence following investigation. Of the total

number of patients reporting a new suspicious symptom,

recurrence was suspected in 56% (n = 152/270). Patients

thus had a 98.1% sensitivity to raising suspicion for a

recurrence based on the reporting of new symptoms with a

99.6% negative predictive value. Our data show that the

efficiency of the current follow-up regime at detecting

suspected recurrence of head and neck cancer is low,

suggesting the need for a customised, more focused follow-

up regime, tailored to individual cases. Patient education

and close relationships with clinicians and allied health-

care professionals are essential for early diagnosis and

management of cancer recurrence. Follow-up regimes

within the first year should be most intensive as recurrence

is most likely within this time, and it serves to alleviate

patient anxiety in the early post-treatment period. More

research needs to be carried out to investigate the role of

patient self-reporting and surveillance of cancer recurrence.

Keywords Head neck cancer follow-up �Self-reporting � Surveillance � Outpatient

Introduction

The optimal follow-up regime for cancer patients has been

a long-standing question [1–3].The premise that a routine

follow-up regime facilitates the early detection and treat-

ment of cancer recurrence has been investigated in large

case series in several cancer fields [1, 4–8]. These studies

vary in their view of whether regular, routine, long-term

follow-up regimes are of limited benefit or not in terms of

increased patient survival. De Visscher et al. [4] concluded

from the analysis of a cohort of 428 patients that routine

patient follow-up regimes were indispensible, but the

length of time was tumour dependent. Boysen et al. [1]

have shown in a prospective study of 661 patients that

P. Kothari � A. Trinidade (&)

Department of Otolaryngology, Luton and Dunstable Hospital,

Lewsey Road, Luton LU4 0DZ, UK

e-mail: [email protected]

R. J. D. Hewitt � P. O’Flynn

University College London Hospital, London, UK

A. Singh

Northwick Park Hospital, Middlesex, UK

123

Eur Arch Otorhinolaryngol (2011) 268:1191–1200

DOI 10.1007/s00405-010-1461-2

routine follow-up regimes are rarely indicated beyond the

third year post-treatment, and that 61% of patients with

recurrence reported their symptoms. They recommend a

focus on patient education in recognition of the signs and

symptoms or recurrence. Conversely, in a more recent

study, Lester et al. [5] concluded that based on the local

prospective data of 676 patients and published evidence,

laryngeal primaries should be followed up for 7 years,

whilst oropharyngeal and hypopharyngeal primaries should

be followed up for 3 years. They also felt that relying on

good patient education for the detection of recurrence

through self-presentation was an unacceptable practice, as

it would lead to the detection of less than two-thirds of

recurrences [5].

The issue is further highlighted by the financial impli-

cations of long-term follow-up for health-care trusts and

patients alike. The cost of medical, allied health-care,

nursing and clerical staff, in addition to patient costs

incurred in accessing the service, is considerable. The

question of whether the time commitment and psycholog-

ical stress involved in such regular clinic visits by patients

is warranted must also be taken into account.

At present, there are three main national guidelines

available in the UK that outline suggested follow-up

regimes for head and neck cancer patients: (1) the con-

sensus document of the British Association of Otorhino-

laryngologists and Head and Neck Surgeons (BAO-HNS),

(2) the Scottish Intercollegiate Guidelines Network (SIGN)

guidelines, and (3) the National Institute for Clinical

Excellence (NICE) guidelines [9–12] (Table 1). This

study’s main focus is on clinician-suspected recurrences of

disease rather than actual recurrences. It aims to determine

how early cancer recurrence is most likely to be identified

by the clinician at a routine outpatient visit, or by the

patient who notices a new symptom.

Setting

The study was conducted across three northwest London-

based head and neck cancer units: the University College

London Hospital (UCLH), Northwick Park Hospital (NPH)

and Mount Vernon Hospital (MVH). The three hospitals

serve as the main centres for head and neck cancer man-

agement for a catchment population of approximately

1.7 million. UCLH and NPH serve as the tertiary referral

and surgical centres where patients are first seen and

diagnostics and surgery are performed. MVH is the onco-

logical centre. The population includes several areas with a

high deprivation index. Patients with head and neck cancer

are under the care of otorhinolaryngology, head and neck

surgery (ORL-HNS), oral and maxillofacial surgery

(OMFS) and oncology. Consultants and allied health pro-

fessionals from all three hospitals participate in a weekly

joint multidisciplinary meeting held via videoconferencing.

Patients and methods

The study was conducted between January 2007 and

October 2007: 1,039 consecutive patients attending the

outpatient department who were undergoing multidisci-

plinary, multimodality management for head and neck

cancer were prospectively collected. Data included patient

age, original stage of cancer, treatment, patient-reported

symptoms and signs, clinician-reported symptoms and

signs and established follow-up plan. A ‘suspicion of

recurrence’ was defined as a sign or symptom noticed by

either the patient or the clinician that led to further inves-

tigation into whether the patient’s cancer had recurred.

These signs and symptoms were often disease specific and

included new onset of dysphonia and/or dysphagia, a new

Table 1 Summary of UK national guidelines for follow-up of head and neck tumour patients

Governing

body

Guidelines

BAO-HNS (1998) Squamous cell carcinoma (SCC): 2–4 weeks post-radiotherapy; year 1, every 1–3 months; year 2, every 2–4 months;

year 3 and 4, every 6 months; discharge at the end of year 5

Adenoid cystic carcinoma: as for SCC, but 6 monthly after year 4 until year 10

Pleomorphic adenoma: 2–4 weeks post-treatment; 6 monthly once effects of surgery ± radiotherapy have settled; discharge at

the end of 5 years

(2002) All guidelines remain unchanged, except for pleomorphic adenoma: monthly follow-up in year 1, decreasing to annually

by year 5 with option of annual visits offered to patients following this

SIGN (2006) Patients to be seen frequently and regularly within first 3 years post-treatment. Based on study by Boysen et al. [1], which

concludes that follow-up on a regular basis is rarely indicated beyond the third year. Follow-up should be limited to patients

where treatment options still remain [13, 14]

NICE (2004) Regular examinations in the first 2 years post-treatment with periods increased between consultations; discharge to be

considered at year 5

1192 Eur Arch Otorhinolaryngol (2011) 268:1191–1200

123

neck lump, new pain within the aerodigestive tract or neck

or positive nasendoscopic findings. All patients underwent

a full examination of the head, neck, oral cavity and

pharynx by a specialist surgeon, which included a routine

nasendoscopic examination. All data, suspicion of recur-

rence and appointment status (whether routine or patient

requested) were collected for all 1,039 patients and entered

into a standard proforma, from which data were later col-

lated and analysed (Appendix 1). A non-validated survey

was also conducted on the final 263 consecutive patients

attending the outpatient setting during the study period

regarding various aspects of their outpatient follow-up

experience, which the authors felt were relevant to this

study (Appendix 2). It was not conducted on the other

patients, as the idea of conducting the survey only occurred

to the authors towards the end of the study period. All data

were analysed using SPSS for Windows statistical package

(SPSS Inc., Chicago, IL, USA) and Microsoft Excel 2007.

Ethical considerations

All data were collected routinely as part of the clinical care

of the patients. No patient records or extra patient data

were accessed, and all collected data were anonymised

before analysis. The survey was reviewed by the ethics

department before distribution.

Results

Demographic data

Approximately, three-quarters of the population were male

(M = 763, 73.4%; F = 276, 26.6%), the overall average

patient age being 62 years (M = 62; F = 59). The youn-

gest patients were 19-year-old males with T3N3M0 naso-

pharyngeal carcinoma (n = 6), and the oldest patient was a

96-year-old male with T3N0M0 oropharyngeal carcinoma.

Tumour type and treatment data

The most common cancer was glottic (n = 369, 35.5%),

followed by oropharyngeal (n = 168, 16.2%) and naso-

pharyngeal (n = 100, 9.6%) (Fig. 1). Most tumours found

were classified as T2 (n = 293, 28%), followed by T3

(n = 275, 26.5%), T4 (n = 223, 21.5%), T1 (n = 177,

17%) and T9 (n = 18, 1.7%). The TNM classification for

all tumours in this study are shown in Table 2. One-quarter

of patients had surgery as their primary modality of treat-

ment (n = 260, 25%); 356 (n = 34.3%) underwent radio-

therapy and/or chemotherapy; 420 (n = 40%) underwent

both modalities.

Tumour recurrence and outpatient follow-up data

The mean follow-up period of our patients in the outpatient

department was approximately 40 months (3.34 years)

following completion of treatment, regardless of modality.

Most follow-ups were routine (n = 951, 91.5%) and the

remainder were patient-requested appointments (n = 88,

8.5%).

Overall, the rate of suspected recurrence of cancer

during the study period was 15% (n = 156/1,039). Glottic

cancer was the most commonly suspected site of recur-

rence (n = 62, 40%) (Fig. 2). When suspected recurrence

was stratified by treatment modality, it was found to be

most common in those patients who had undergone surgery

and adjuvant chemoradiotherapy (n = 72, 46%). When

stratified by original disease stage, T2 tumours were found

to be most commonly suspected of recurrence (n = 43,

28%) (Table 3). Of the suspected recurrences, 64 (56%)

were suspected within the first year of follow-up, followed

by 21 (14%) in the second year and 23 (15%) in the third

year. The overall trend was a decrease in suspicion of

recurrence with time, dropping to 6% (n = 10) by the

fourth year (Fig. 3). The shortest follow-up period until a

recurrence was suspected was 2 months for oropharyngeal

cancer (n = 2). Both patients had macroscopically clear

surgical margins at the time of operation. Histology and

radiology supported this post-operatively, and both patients

were deemed to be disease free following adjuvant therapy.

This strengthened the case against the possibility of this

representing residual or persistent disease as opposed to

recurrence given the short period of time.

The longest was 220 months (18.3 years) for laryngeal

cancer (n = 4). In the case of the latter four patients, none

was part of a routine follow-up regime, but requested an

appointment reporting a change in their voice. Again, given

the length of time to new findings, it is possible that these

patients could have developed second primary tumours as

opposed to recurrences. However, both can be considered

Fig. 1 Distribution of primary cancer site by type

Eur Arch Otorhinolaryngol (2011) 268:1191–1200 1193

123

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123

as ‘new cancer events’. The authors felt that such distinc-

tion would have made little difference in the overall

treatment decisions proposed at the time of discovery and

considered them as recurrences in view of their individual

past oncological histories.

Of those patients routinely seen, 10% (n = 96/951)

were suspected of having a recurrence. Of those patients

requesting an appointment to report new or changing

symptoms, the suspicion rate of recurrence rose to 68%

(n = 60/88). The sensitivity of a patient’s reported symp-

toms, resulting in a clinician’s suspicion of recurrence, was

thus 98.1% (152/155), with a specificity of 86.6% (766/

884). The probability of a suspected recurrence occurring

in a patient who had reported symptoms (PPV) was 56.3%

(152/270). However, the probability of a clinician having

no suspicion of recurrence in an asymptomatic patient

(NPV) was 99.6% (766/769) (Table 4). Of the asymp-

tomatic patients attending a routine follow-up regime, only

three (0.3%) were suspected of having a recurrence (two

nasopharyngeal, one glottic), and two (0.2%) were found to

have an actual recurrence on investigation (glottis and

nasopharynx).

Regarding the patient survey, 67% (n = 176/263) of

patients felt that the multidisciplinary team (MDT) clinic

met the goals they hoped would be achieved during their

visit. Of all, 84% (n = 221/263) of patients felt that their

head and neck follow-up visits were too frequent; 60%

(n = 159/263) of patients were also booked to see an allied

health professional in addition to the attending clinician on

their day of attendance to the clinic. Of these, 84%

(n = 134/159) felt that issues addressed at follow-up with

the clinician overlapped or duplicated those addressed by

the allied health-care professionals. When asked about their

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Fig. 2 Distribution of tumour types by suspicion of recurrence

Table 3 Suspicion of recurrence stratified by treatment modality and

original tumour stage

n (%)a

Treatment modality

Surgery ? chemoradiotherapy 72 (46)

Chemoradiotherapy 35 (22)

Radiotherapy 29 (19)

Surgery 18 (12)

Chemotherapy 2 (1)

Original tumour stage

T9 2 (1)

T1 26 (17)

T2 43 (28)

T3 40 (26)

T4 36 (23)

Data not available 9 (6)

a Total = 156

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Time to suspicion of recurrence (years)

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Fig. 3 Overall suspected

recurrences from completion of

treatment with respect to time

(years)


123

opinion of a less intensive follow-up system based on

patients reporting problems and requesting appointments,

73% (n = 192/263) were in favour of it. When asked who

they would like to contact first in such a system, most

patients (n = 118/263, 45%) stated a clinical nurse spe-

cialist, followed by the medical secretary (n = 58/263,

22%). Clinicians ranked third (n = 42/263, 16%). Other

contacts included a speech and language therapist (n = 21/

263, 8%), their GP (n = 18/263, 7%) and a dietician

(n = 5/263, 2%).

Discussion

This study stemmed from the authors’ belief that there was

a dichotomy between the historic follow-up regime of head

and neck patients currently employed in the UK and the

more recent introduction of a multidisciplinary approach to

its management. The latter seems to have evolved in par-

allel to the former, instead of having been effectively

integrated into it, therefore allowing itself to the possibility

of multiplicity and repetition in patient follow-ups with the

surgeon and the various allied health-care professionals

who act independently of the surgeon and deal with the

various aspects of post-treatment rehabilitation. These

include clinical nurse specialists, speech and language

therapists, dieticians and, where appropriate, palliative care

nurses. Their input ensures a more holistic patient

approach, and many rehabilitative issues traditionally dis-

cussed with the surgeon are more efficiently addressed

through their own individual systems.

The guidelines outlined in Table 1 differ in their advice

as there is currently no high-level evidence to support any

one given regime, and many variations exist from region to

region [5, 13]. The authors believe that a streamlining of

the current system to a more modern, efficient one that

takes into account geographical variations and individual

patient requirements is needed.

From our data, the average age, sex ratio and distribution

of our population are similar to other data published else-

where in literature and is therefore a representative popu-

lation of adults with head and neck cancer. The data suggest

that the reporting of new symptoms by a patient provides a

very sensitive predictor for the suspicion of a recurrence. In

turn, this suggests that a less rigid, patient-oriented system

would have a very low chance of missing patients with a

suspected recurrence. The introduction of such a system

would require patient education of the symptoms and signs

of recurrence. Patients unable to achieve this would need to

be readily identifiable and managed accordingly. Allied

health-care professionals will also play an important role in

addressing other arising issues.

The efficacy of the current routine follow-up regime in

our institution at detecting a suspected recurrence is 10

versus 68% in follow-ups concerning patient-reported

symptoms. This suggests the need for a more focused

follow-up regime. It again suggests that the patient rather

than the clinician is better able to identify a suspected

recurrence and therefore facilitate early detection.

Three patients within a routine follow-up regime were

suspected of having a recurrence and, on investigation, two

of them were confirmed to have recurrence. These patients

represent the most difficult cases of recurrence for the

clinician to identify and therefore a possible limitation of a

less rigid, patient-oriented system as they would potentially

be overlooked in the initial stages of disease when their

treatment options would be greatest.

A clear definition of recurrence versus persistence of

disease is desirable in the management of head and neck

cancer and its follow-up. The authors accept that micro-

scopic disease can remain even in the face of negative

random biopsies of the macroscopically clear surgical

margins, representing persistent disease rather than a

recurrence. However, no uniform criteria to define a clear

surgical margin exist among practising head and neck

surgeons and the definition of a clear tumour margin after

chemoradiation is unclear. Most surgeons rely on frozen

section, but this view is not held by all [14].

Whilst not validated, the results of the survey are

interesting as they provide an insight into the patients’

perspective of the current follow-up regime. Research

suggests that the incidence of patients’ under-reporting

symptoms and signs is far increased with more frequent

follow-up [1]. In general, patients felt that being seen

intensively for the first year, then having visits tapered off

over the next 2 years and finally being seen according to

symptoms thereafter was appropriate and felt that this

represented an overall better system. Most felt that overall,

visits were too frequent and intensive and felt that different

aspects of the MDT clinic needed to communicate better to

avoid replication. The authors stress that whilst these data

can by no means form the sole basis for implementing

Table 4 Statistical analysis of

patient-reported new/changing

symptoms versus clinician-

suspected recurrence rates

Suspected

recurrence

No suspected

recurrence

Total

Patient reporting symptoms 152 118 270

Asymptomatic patient 3 766 769

Total 155 884 1,039


123

changes into current follow-up regimes, it does suggest that

an updated system might take into consideration an indi-

vidual patient’s attitude to his or her disease when tailoring

the follow-up plan.

Comparison with other studies

Our data are similar to those of Boysen et al. [1] (see

Fig. 3), showing a marked reduction in suspected recur-

rence after the third year. This seems to support their claim

that in general, routine follow-up regimes are rarely indi-

cated after the third year. However, four patients were

suspected of recurrence of laryngeal cancer at 220 months;

therefore, seemingly supporting claims by Lester et al. and

Spector et al. [5, 15] that laryngeal primaries should be

followed up for 7 years. Marchant et al. [16] suggest that

follow-up for life should be considered if detrimental

habits such as smoking and alcohol use persist. However,

these four patients were not routinely seen over

220 months, but instead requested an appointment to have

new symptoms reviewed. It therefore supports an argument

against routine follow-up regimes for such an extended

length of time. Nonetheless, this study does not have a

sufficiently large population number to accurately delineate

specific subsets of patients, but the authors feel that it does

highlight the need for flexibility in any chosen system of

follow-up. In a large chart review of 2,550 patients, again

by Spector et al. [16] it was found that the incidence of

distant metastases in squamous cell carcinomas of the

larynx and pharynx was greatest between 1.5 and 6 years

after initial treatment with the mean incidence being less

than or equal to 3.2 years. Our data support this claim.

They also found that delayed and distant lymph node

metastases were significantly higher in advanced primary

disease (T4 stage), locoregional recurrences and regional

disease (N2 and N3) in both the larynx and hypopharynx,

and that metastases occurring in hypopharyngeal tumours

were three times greater than in laryngeal cancers [16].

Regarding the importance of patient education and can-

cer detection in the follow-up system, there is conflicting

evidence as to whether patient surveillance versus routine

clinic surveillance results in a survival advantage [4, 5, 17,

18]. Some authors claim that up to two-thirds of recurrences

can be detected through increased patient self-awareness

[1, 4]. Lester et al. [5] state that this level of detection is

unacceptable. Our data of a sensitivity of 98.1% and an

NPV of 99.6% suggest that patient surveillance is not only

an acceptable measure of cancer recurrence, but a highly

sensitive and specific one that could potentially be incor-

porated into follow-up regimes that are tailored based on the

MDT’s perceived reliability of an individual patient’s

likelihood to report symptoms and signs.

Clinical applicability of this study

The authors feel that this study supports the notion of an

intensive follow-up regime for the first year post-treatment

for all cancers. It also suggests that intensive follow-up

after 3 years is not necessary. Patient education still plays

an important role in identifying recurrence of disease and

placing emphasis on this will allow for a more flexible

approach to follow-up, especially beyond 3 years post-

treatment. Once appropriately educated, patients can con-

tinue to bring worrisome symptoms to the clinicians’

attention, even many years post-treatment, without detri-

ment to overall care. Fostering a truly multidisciplinary

approach, involving greater patient responsibility to allied

health-care professionals and increased patient access to

members such as the clinical nurse specialist, would also

complement such a service, avoid repetition and, based on

the survey, approximate the service closer to patients’

expectations.

Limitations of this study

This study does not confirm that self-reporting is the best

follow-up method, but does suggest that this is a potential

area of study. Another limitation is that our sample size

precludes subset analysis. There were 18 patients identified

with unknown primaries in our population (see Table 2).

These patients pose a special problem as they do require

close monitoring and thus represent a confounding factor

of our study. However, it is still not known whether such a

follow up regime confers any benefit, and further research

into this subpopulation is needed. Disease-specific survival

data were not available. Finally, the survey used in this

study, though yielding interesting data, was non-validated.

Conclusion

Follow-up policies for head and neck cancer patients must

necessarily vary from centre to centre and must be the

product of agreed local practice and distinctive population

demographics. A shorter, flexible, individualised, inte-

grated multidisciplinary approach would seem to be more

favourable than a lengthy, prescriptive one that encour-

ages clinicians to practise independently of the rest of the

MDT. The result would be less over-subscribed clinics

and better-informed, less anxious patients with individu-

ally tailored follow-up regimes and greater clinic access if

needed.

Conflict of interest None to declare.


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Appendix 1: Data collection proforma

Date of consult: DD/MM/YYYY

Age: Sex:

Primary site: Oral Cavity Oropharynx Supraglottis Glottis

Hypopharynx Thyroid Salivary Gland Sinonasal

Nasopharynx Unknown Primary Other _____________

T: N: M:

Patient seen by: Surgeon Oncologist

Treatment completion date: Surgery: DD/MM/YYYY

Radiotherapy: DD/MM/YYYY

Chemoradiation: DD/MM/YYYY

Current follow-up plan (months): 1 2 3 6 12 Discharged

Routine follow-up? Yes No If no, requested by who? _________

Patient reported symptoms? No Yes If yes, symptom? _______________

Clinical findings: No recurrence Suspicion of recurrence

Management decision: Imaging EUA/Bxa Reassurance

Additional consult by: Dietitian SALTb CNSc Palliative care

Other _________________

Proposed follow-up plan (months) 1 2 3 6 12 Discharge

Comments: __________________________________________________________________________

a Examination under anaesthesia / biopsy

b Speech & Language Therapist

c Clinical Nurse Specialist


123

Appendix 2: Patient survey

1. How do you view the number of follow-up visits you make to the head and neck clinic?

Too frequent Just about right Not frequently enough No opinion

2. Are you being seen by anyone else in the head and neck clinic today besides the doctor?

Clinical nurse specialist

Speech & Language Therapist

Dietitian

Dental/Oral hygienist

Other Please state who:________________________

None

3. If you are seeing someone else besides the doctor, do you think that the issues usually covered with

them overlaps with or duplicates the issues covered with the doctor?

Yes No Don’t know Not applicable

4. Do you feel that by coming to this clinic , you are able to adequately resolve any issues you may

have?

Yes No Don’t know

5. Would you prefer a less intensive follow-up sy stem that based on you reporting any problems and

requesting an appointment?

Yes No Don’t know

6. If you prefer such a system, who would you like to contact in the first instance?

Doctor GP

Clinical Nurse Specialist Speech & Language Therapist

Dietitian Dental/Oral hygienist

Doctor’s secretary

Other Please state who:__________________________


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The follow-up of patients with head and neck cancer: an analysis of 1,039 patients

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