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  Volume 95
Numero 2
marzo-aprile 2009 		I documenti sono in formato PDF, consultabili utilizzando Acrobat Reader
 
Incidence of invasive cervical cancer and direct costs associated with its management in Italy

Alessandro Ricciardi, Nathalie Largeron, Paolo Giorgi Rossi, Mimma Raffaele, Catherine Cohet, Antonio Federici, Fabio Palazzo
1Agency for Public Health, Lazio Region, Rome, Italy; 2Sanofi Pasteur MSD, Lyon Cedex 07, France; 3INRCA, Department of Medical Oncology, Rome; 4National Research Council, Institute of Research on Population and Social Policies, Rome, Italy

Key words: cervical cancer, cost, human papillomavirus, Italy.

abstract

Aim and background. Cervical cancer is the second most common cancer in European women aged 15-44 years. The aim of this study was to estimate the direct cost of managing invasive cervical cancer in Italy.
Methods. Data from the Italian Network of Cancer Registries were used to estimate the annual number of new cervical cancer cases. To assess the management costs, a typical management pathway for each FIGO (Fédération Internationale de Gynécologie et d’Obstétrique) cervical cancer stage was derived from published guidelines. Data from the Modena Cancer Registry were used to estimate the proportion of patients by FIGO stage. This algorithm was combined with tariffs for outpatient and inpatient procedures to obtain a mean cost for each FIGO stage.
Results. An estimated 2,927 new cases of cervical cancer occurred in Italy in 2005 (crude incidence 9.7/100,000; world age-standardized incidence 6.0/100,000). The estimated numbers of new cases by FIGO stage were: FIGO I, 1,927; FIGO II, 556; FIGO III, 259; and FIGO IV, 185. Costs for the most frequent procedures were estimated as: € 6,041 for radical hysterectomy or other surgery; € 4,901 for radio-chemotherapy; € 1,588 for bra­chy­therapy; and € 3,795 for palliative chemotherapy. Mean management costs for incident cases (including 10 years of follow-up) were estimated at: FIGO I, € 6,024; FIGO II, € 10,572; FIGO III, € 11,367; FIGO IV, € 8707; and € 5,854 for the terminal phase (1 month). The total direct management cost was estimated at € 28.3 million per year.
Conclusions. This is one of the first studies to estimate the direct cost of treating patients newly diagnosed with invasive cervical cancer in Italy. Although according to current management pathways real treatment costs are likely to be underestimated, this information is necessary to design evidence-based vaccination policies able to harmonize primary and secondary prevention of cervical cancer.

Introduction
Cervical cancer is the second most common cancer in women worldwide1. It is estimated that 500,000 women are diagnosed with cervical cancer each year and more than 50% die from the disease1. Although most cervical cancer cases are observed in developing countries, each year in Europe more than 33,000 new cases occur and approximately 15,000 women die from the disease1.
Almost 100% of cervical cancers are caused by infection with human papillomavirus (HPV)2,3. To date, more than 100 different types of HPV have been identified, of which an estimated 40 are known to infect the genital tract4. HPV are classified according to their ability to induce malignant transformation of infected cells: high-oncogenic risk types are predominantly associated with the development of malignancies (such as cervical, vaginal, vulvar or anal cancers), and low oncogenic-risk types usually cause more benign lesions (e.g., genital warts)5. Although several HPV types are involved in the development of cervical cancer, HPV-16 and HPV-18 account for most (70%) of the cases6. Data from recent studies show that HPV-16 and HPV-18 also account for approximately 75% of all cases of invasive cervical cancer in Italy7,8.
Until recently, only secondary prevention strategies, such as cervical cancer screening using the Pap smear test, have been available for cervical cancer. Screening using the Pap smear test enables precancerous lesions to be identified and treated. However, secondary prevention is only effective for those women who are screened regularly9,10. Although cervical cancer screening has been shown to greatly reduce the incidence of cervical cancer, many women are still dying from the disease, even in countries with widespread screening programs and high levels of coverage11,12.
With the recent introduction of vaccines against HPV, many European countries, as well as the USA and Australia, have implemented nationwide HPV vaccination programs for adolescents to prevent cervical cancer and HPV-related diseases. Although national vaccination strategies are starting in Italy, it is important to assess the burden of cervical cancer. Italy does not currently have a national cancer registry, but some local registries do exist. Health care is under the responsibility of regional governments, leading to a lack of standardized collection of health care information, which is stored in local health care data bases.
Given the absence of a centralized source of data, the aim of this study was to estimate the annual incidence of invasive cervical cancer and to assess costs associated with its treatment and patient management in Italy.
Material and methods
Annual number of new cases of invasive cervical cancer in Italy
In the absence of national cancer registry data, we estimated the annual number of incident cases of invasive cervical cancer in Italy using age-specific incidence rates provided by the Italian Network of Cancer Registries (Associazone Italiana Registri Tumori; AIRTum) for the period 1998-200213. The AIRTum includes 26 population-based registries that cover approximately 15 million resident Italians (26% of the total population). We applied these rates to the Italian general female population in 2005 (Istituto Nazionale di Statistica)14 to obtain the annual number of cervical cancer cases. We also used an alternative approach by applying the AIRTum incidence rates stratified by geographical macro-area.
FIGO stage of cervical cancer at diagnosis
The progression of invasive cervical cancer was staged using the Fédération Internationale de Gynécologie et d’Obstétrique (FIGO) classification15. To estimate the number of cases of invasive cervical cancer by FIGO stage, 436 staged cancers that were reported between 2002 and 2004 and were registered with the Modena Cancer Registry16 (missing cases corresponding to 4.4%) were considered. The Modena Cancer Registry reports the most up-to-date and comprehensive data among the Italian cancer registries having information on cancer stage.
Management and costs of invasive cervical cancer
To assess the mean cost of invasive cervical cancer, we defined a typical disease management pathway for each FIGO stage (including the terminal phase). International and local guidelines for the management of women with cervical cancer were selected through a PubMed search. Medical Subject Headings terms such as “uterine cervical neoplasms” and “practice guidelines” were used. Guidelines from the Istituto Toscano Tumori17 were identified as the most comprehensive and accepted basis to define typical disease management pathways.
For outpatient procedures, we used tariffs included in the National Tariff Formularies18. For inpatient procedures, we identified the appropriate diagnosis-related group tariffs for the Lazio region. The unit costs for surgical treatments (mainly conization and radical hysterectomy) were estimated using the average of the reimbursement fees actually used in the Lazio Hospital Discharge Registry (on the basis of the ICD-IX-CM code). The overall annual direct cost of new invasive cervical cancers in Italy was estimated by multiplying the mean cost per FIGO stage by the number of cases in each stage.
Results
Annual number of new cases of invasive cervical cancer in Italy
According to the most recent and comprehensive data from the AIRTum, the crude incidence of invasive cervical cancer in Italy is 9.7 per 100,000 (7.7 per 100,000 when standardized on the European population). Applying this rate to the resident female population, it was estimated that there were 2,927 new cases of invasive cervical cancer in Italy in 2005. Extrapolation using data stratified by geographical macro-area provided an estimated 2,806 cases (incidence rates of 8.5; 7.4; and 6.4 per 100,000 standardized on the European population for the north, center and south, respectively), whereas the latest available GLOBOCAN estimate from the International Agency for Research on Cancer (IARC) 1 for the year 2002 was 3,418 new cases. Table 1 shows the age-stratified incidence and number of new cases. Furthermore, for Italy in 2002, GLOBOCAN gave an estimated 1,186 deaths1.

Table 1 - Age-stratified incidence and number of new cases of cervical cancer in Italy, 2005 (based on AIRT data 1998-2002 and ISTAT 2005)

Age group

Incidence

Italian female

New cases cancer

 

per 100,000

population

of cervical

 

 

 

 

0-4

0

1,331,063

0

5-9

0

1,303,603

0

10-14

0.1

1,379,026

1

15-19

0.1

1,404,389

1

20-24

0.4

1,570,091

7

25-29

2.8

1,938,484

55

30-34

6.1

2,289,167

139

35-39

11.2

2,392,657

268

40-44

14.2

2,286,308

325

45-49

15.2

2,015,641

307

50-54

14.4

1,887,488

272

55-59

15.0

1,917,781

287

60-64

14.7

1,707,702

250

65-69

14.5

1,727,599

251

70-74

14.7

1,594,401

235

75-79

16.7

1,400,564

234

80-84

16.4

1,117,123

182

85+

13.6

822,484

112

 

 

 

 

Total

9.7

30,085,571

2927


Stage of cervical cancer at diagnosis
The proportion of each FIGO stage drawn from the Modena Cancer Registry (on the basis of 436 cases registered between 2002 and 2004) was applied to distribute the estimated 2,927 incident cervical cancer cases by stage. This resulted in an estimated 1,927 women diagnosed with FIGO stage I (719 IA1; 306 IA2; 619 IB1 and 283 IB2), 556 women diagnosed with FIGO stage II (171 IIA and 385 IIB), 259 women diagnosed with FIGO stage III, and 185 women diagnosed with FIGO stage IV (74 IVA and 111 IVB).
Management and costs of invasive cervical cancer
The treatment algorithm is shown in Table 2. It was assumed that most patients diagnosed with FIGO stages from IA1 to IIA would undergo a surgical procedure: conization for stage IA1 or radical hysterectomy for the other stages. For FIGO stages from IIB to IVA, it was assumed that treatment included radio-chemotherapy or brachytherapy. It was assumed that all patients in stage IVB would receive palliative chemotherapy for 6 months and 20% of them would also receive radiotherapy and palliative surgery. The algorithm also included management during a follow-up period of 10 years post-diagnosis.



According to the proposed management algorithm, the cost of palliative care for terminally ill patients included 1 month of hospitalization. It is known that about 90% of patients dying of cancer go through this terminal phase19. Therefore, the costs associated with the terminal phase were applied to 90% of all annual cervical cancer deaths (n = 1,069), as estimated by the IARC1.
The unit costs associated with each procedure are given in Table 3. The unit cost for radio-chemotherapy combines the costs of chemotherapy and radiotherapy. The cost of chemotherapy was obtained from the Italian specific diagnosis-related group tariff, whereas the cost of radiotherapy was derived from a combined profile of ambulatory procedures including 11 different ICD-IX-CM codes. Finally, it was assumed that all patients would undergo laboratory analyses, with a cost ranging from €98 for early stage IA to €472 for stage IVB (Table 3).

Table 3 - Unit costs for procedures to treat cervical cancer

Procedure

Unit costs (€)

 

 

Conization (ambulatory)

908.58

Conization (full hospitalization)

3,125.41

Radical hysterectomy (including pelvic lymph

 

node dissection and para-aortic

 

lymph node sampling)

6,040.63

Radio-chemotherapy

4,900.73

Palliative chemotherapy

3,794.89

Brachytherapy

1,587.98

Palliative surgery

6,040.63

Hospitalization

2,668.82

Hospice care for terminal phase (per day)

195.15

Gynecologic examination

13.63

Pap test

11.16

Colposcopy

10.74

Echography

30.99

Computed tomography

88.31

Laboratory analyses (IA)*

97.67

Laboratory analyses (IB to II)*

383.54

Laboratory analyses (III and IVA)*

552.42

Laboratory analyses (IVB)*

417.85

 

 

*Laboratory analyses include for all stages: a range of blood biochemistry and hematology tests, visual examination, thoracic X-ray, bimanual pelvic examination. For stages IB to IV they also include the costs of cystoscopy, flexible sigmoidoscopy and urography. For stages III and IV computed tomography or magnetic resonance imaging are also included (50% respectively).


The estimated mean costs per patient (including follow-up and terminal phase) were as follows: €6,024 for FIGO stage I (€5,256 in the first year); €10,571 for FIGO stage II, (€8,914 in the first year); €11,367 for FIGO stage III (€9,710 in the first year); €8,707 for FIGO stage IV; and finally €5,854 for patients in the terminal phase (Table 4). The weighted mean cost of cervical cancer management was estimated to be €9,569 per patient. The total cost to the Italian health care system of managing 2,927 patients with invasive cervical cancer, including follow-up and terminal phase, was estimated to be €28.1 million. This estimate could decrease to €27.3 million when applying our cost estimates to the 2,806 cases obtained using data stratified by geographical macro-area and increase up to approximately €33.0 million when applying our cost estimates to the 3,418 cases reported by GLOBOCAN for Italy in 2002.

Table 4 - Total and unit costs of newly diagnosed cervical cancer during the first year of treatment and including follow-up and terminal phase

FIGO stage

Cases

Excluding follow-up & terminal phase

Including follow-up & terminal phase

 

 

 

 

 

 

 

 

Total cost (€)

Unit cost (€)

Total cost (€)

Unit cost (€)

 

 

 

 

 

 

FIGO I

1, 927

10,128,219

5,225.95

11,610,048

6,024.93

  I A1

719

2,015,845

2,803.68

2,432,578

3,383.28

  I A2

306

1,878,321

6,183.30

2,055,679

6,717.90

  I B1

619

4,249,583

6,865.24

4,668,380

7,541.83

  I B2

283

1,984,470

7,012.26

2,453,412

8,669.30

FIGO II

556

4,956,213

8,914.05

5,877,527

10,571.09

  II A

171

1,282,899

7,502.33

1,566,253

9,159.37

  II B

385

3,673,314

9,541.08

4,311,274

11,198.12

FIGO III

259

2,514,878

9,709.96

2,514,878

11,367.00

FIGO IV*

185

1,610,764

8,706.83

1,610,764

8,706.83

  IV A

74

718,537

9,709.96

718,537

9,709.96

  IV B

111

892,228

8,038.09

892,228

8,038.09

Terminal phase

1,069

 

 

6,258,461

5,854.50

All phases

2,927

19,210,075

6,536.06

28,300,852

9,668.89

 

 

 

 

 

 

*The cost of treatment for stage IV included the terminal phase; no follow‑up was considered, as it was assumed that death occurred during this time.


Discussion
Various studies have assessed the incidence and mortality of cervical cancer in individual regions of Italy20-23. AIRTum has assessed the epidemiology of diseases at a national level13. To our knowledge, however, this is one of the first studies designed to estimate the annual incidence of invasive cervical cancer by tumor stage for the whole of Italy and to assess the associated health care costs. We estimated that there were 2,927 new invasive cervical cancer cases in Italy in 2005, with a crude incidence of 9.7 per 100,000. The mean cost per case borne by the National Health Service was €9,669. Applying an extrapolation from the cancer registries data based on geographical distribution, we obtained a slightly smaller number of cancer cases (2,806 cases), this being mostly due to a lower incidence in the south of Italy.
The number of new cases of invasive cervical cancer estimated in this study is lower than the 3,418 cases estimated for Italy by the IARC in GLOBOCAN1. However, it should be noted that GLOBOCAN presents estimates for all cases of cervical cancer in the year 2002 based on the populations of different countries in the middle of that year, although the disease rates are not those for 2002, but have been drawn from the most recent registry data available. In the case of Italy, this data was for the period 1993-1997.
Our estimated crude incidence rate of 9.7 per 100,000 is also slightly lower than the crude rate of 11.6 per 100,000 population reported by GLOBOCAN for the year 2002, based on the 1993-1997 incidence data. Nevertheless, it is within the range of age-standardized rates reported in GLOBOCAN for the United Kingdom, France and Germany1. The distribution of incidence by age in Italy is also comparable to the global trend for the disease: beginning at age 25 years, incidence rates increase until 45 years of age, when they reach a plateau1.
Although this study represents an extensive and rigorous analysis of available data sources, there are a number of limitations. The results are based on data from diverse regional cancer registries that represent only about 26% of the population of Italy but which have been scaled up to the whole female population. Furthermore, the AIRTum collects data from 26 cancer registries that provide a good reflection of disease incidence in central and northern Italy but a worse representation of disease incidence in southern Italy. The estimates also assume that the incidence of cervical cancer has been stable over time and thus do not take into account the decrease in cancer rates that can result from organized screening programs 24,25, which has been observed in Umbria and central Italy22,23. Moreover, the coverage of screening programs is better in northern and central Italy than in southern Italy26, and incident cancer rates may therefore remain higher in southern Italy.
The mean treatment cost of €9,669 for incident cervical cancer is lower than estimates recently reported for France (€13,509) and the UK (£10,464; approximately €13,612)27,28. As the mean cost per patient increases with cervical cancer severity at diagnosis, the difference is due in part to the different FIGO stage distributions considered in these different studies. As an example, 66% of new cases were considered to be FIGO stage I in the present study, compared with 60% in the French study. In addition, 24.6% of cases in the present study were considered to be FIGO stage IA1, which was associated with a mean cost of only €3,383. Our findings are also lower than other data published recently in Italy. In a study conducted using a hospitalization prevalence method, Marocco et al.29 reported a total cost for cervical cancer of €39.4 million. In another evaluation performed in Italy, the mean cost of cervical cancer management was calculated as €16,70030.
The methods for cost estimation also have limitations, since the algorithms for disease management were based on guidelines for treating cervical cancer patients rather than on data derived from a retrospective analysis of individual case reports, as was used in the French study28. If more information were available on the actual procedures used to treat women with cervical cancer, a more accurate cost for management would have been calculated. However, the approach used in the present study enables costs to be estimated for each disease stage, including rare cases such as FIGO stage IV, which might not be obtained so readily in an observational study.
Extrapolation of the distribution of diagnosis stage to the Italian population as a whole may be questionable, as the FIGO staging was obtained from one single source – the Modena Cancer Registry. Although some other cancer registries in Italy provide information on cervical cancer stages, it was not possible to pool their data since neither a National report nor a disease classification is available. As reported by the AIRTum, the implementation of organized screening programs as well as opportunistic screening practices has led to a high proportion of women diagnosed with invasive cervical cancer that have early stage disease, and the proportion of adenocarcinomas has also increased 13. The area of Modena has had a well-implemented screening program since 1999, whereas in other areas where screening programs are not implemented, there may be a higher incidence of later stage disease and, consequently, a greater treatment cost for cervical cancer. Therefore, our approach of using this registry data can be considered adequate, as it is based on observed data and leads to conservative cost estimates (since it represents a post-screening situation and is likely to under-represent the advanced stages).
A further limitation of the cost estimates is that they mainly account for the costs associated with inpatient treatments. However, the potential outpatient costs, such as repeated physician consultations, and indirect costs of cervical cancer are also considerable. Our results therefore provide an underestimation of the true cost of cervical cancer sustained by the National Health Service.
Conclusions
A rigorous estimation of disease burden is a key element to support decision-making related to the allocation of health care resources for cervical cancer prevention strategies. The introduction of organized screening programs across Italy was mandated in 2004. As a result, most new cases of cervical cancer are diagnosed at early stages of disease13. In addition, the incidence of cervical cancer would be expected to show a significant decrease, as reported for the UK23. Nevertheless, approximately 3,000 new cases of invasive cervical cancer are still diagnosed each year in Italy, leading to an estimated expenditure of €28.3 million (applying the lower incidence estimate, total costs would be 3.5% lower than this figure, whereas applying the most recent GLOBOCAN estimate, costs would be 17% higher).
The present study provides a valuable perspective on the burden of disease which can help in defining and implementing the most cost-effective HPV vaccination policy. Provided that high participation rates are attained, and that inequity in the access to public health interventions is minimized31, the combination of HPV vaccination and cervical screening could significantly reduce the occurrence of cervical dysplasia and, in turn, cervical cancer and associated management costs.

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