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Original Article

Venous thromboembolism: What pharmacists know? What do they need?

J Oncol Pharm Practice 0(0) 1–7 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1078155214560639 opp.sagepub.com

Jean-Baptiste Rey1,2, Nicolas Jovenin3, Pierre Kreit4, Je´roˆme Sicard5, Damien Parent1, Dominique Hettler6,7, Philippe Nguyen8,9 and Jean-Luc Ducrocq10

Abstract Introduction: Venous thromboembolism is common in cancer. Low-molecular weight heparins are recommended for prolonged treatment (3–6 months or more if the cancer is active) and prevention of recurrence of venous thromboembolism in cancer. Community pharmacists are often faced with questions from patients. The main objective of this study was to describe the organization, practices and knowledge of pharmacists in care of venous thromboembolism in cancer patients. Methods: A descriptive survey was conducted electronically in October and November 2013 with pharmacists in the Champagne-Ardenne region. The questionnaire collected data on the general organization of the pharmacy, management of outpatients with cancer and thrombosis, and the level of knowledge regarding recommendations on the management of thrombosis in patients with cancer. Results: The participation rate was 31.6%. In 93% of cases, pharmacists had no particular expertise in oncology and/or supportive care. In addition, 96% did not know the existence of recommendations for ‘‘thrombosis in cancer.’’ Finally, 49% gave the correct answer to the case report (low-molecular weight heparins). Conclusion: Training sessions on the management of venous thromboembolism in cancer are currently available to pharmacists in the region. A new assessment of knowledge will be performed at the end of the year 2014. This regional experience is now extended to a national level (all French regions).

Keywords Pharmacists, thrombosis, cancer, recommendations

Introduction Cancer and thrombosis are frequently associated, as this combination was described in 1865 by Armand Trousseau.1 The relative risk of venous thromboembolism (VTE) (including deep vein thrombosis (DVT) and pulmonary embolism (PE)) in a cancer is estimated at 6.5.2 A total of 15–20% of patients with VTE were also afflicted with cancer.3–7 Finally, VTE is the second leading cause of mortality in cancer.8 Management of VTE in cancer patients is described in the recommendations of: the Institut National du Cancer—French National Cancer Institute (INCA),9 the Agence Nationale de Se´curite´ des Me´dicaments et produits de sante´—French drug agency (ANSM) in 2009, the Association Francophone des Soins Oncologiques de Support (AFSOS) recommendations,10 and the good clinical practices international

recommendations supported by the Groupe Francophone Thrombose et Cancer (GFTC) in 2013. 1

Institut de Cance´rologie Jean Godinot, De´partement de Pharmacie, France 2 Universite´ de Reims Champagne-Ardenne, Faculte´ de Pharmacie – Laboratoire EA4691, France 3 Re´seau Re´gional de Cance´rologie Champagne-Ardenne, France 4 URPS Pharmaciens Champagne-Ardenne, France 5 Pharmacie Principale, Chaˆlons en Champagne, France 6 CHU de Reims, Pharmacie, France 7 ARS Champagne-Ardenne, OMEDIT, Chaˆlons en Champagne, France 8 CHU de Reims, Laboratoire d’He´matologie, France 9 Universite´ de Champagne-Ardenne, Faculte´ de Me´decine, France 10 Leo Pharma, Medical Affairs, Voisins le Bretonneux, France Corresponding author: Jean-Baptiste Rey, Institut de Cance´rologie Jean Godinot, De´partement de Pharmacie, 1, rue du Ge´ne´ral Koenig, 51100 Reims, France. Email: [email protected]

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However, these recommendations are little known and little used despite a broad and free dissemination on media such as the Internet or smartphones. Indeed, in France, as elsewhere, most of the recommendations and standards have not had the desired impact on medical practices.11–13 In these recommendations, low-molecular weight heparins (LMWH) are the treatment of choice in VTE patients with cancer over a period of 3–6 months (or beyond if cancer is active). However, recent studies on the implementation of the ‘‘thrombosis and cancer’’ recommendations conducted in France14,15 showed a broad under-prescription of LMWH in the long term in patients with VTE and cancer, around 50%, regardless of the continent or country where the study was made. On the other hand, there is a wide variability in therapeutic care, whether in the choice of the molecule or the duration of treatment, depending on the type of practice (hospital physicians, general practitioners), or medical specialty (oncology, vascular medicine), or even specific treatment of cancer disease. Finally, given the severity of thromboembolic complications in cancer patients and their very pejorative effect on prognosis, improved use of LMWH at treatment doses in accordance with the recommendations and guidelines appears imperative.16 Along with these two observations (i.e. ‘‘VTE– cancer’’ as a common and serious combination and non-optimal management), the community pharmacist is a key player. On the one hand, he plays a central role in the management of outpatients as a primary healthcare professional, easily accessible, since patients only have to ‘‘push the door’’ of the pharmacy. On the other hand, the HPST law (Loi ‘‘Hoˆpital Patients Sante´ Te´rritoires’’)17 clarifies the role of pharmacists: primary care actor, cooperation with health professionals, public service mission, continuity of care, therapeutic education,a . . . missions that pharmacists are willing to assume. Finally, French ‘‘Cancer plans’’ 2 and 318,19 solicit pharmacists in the ‘‘field of the counseling and information regarding drug interactions and side effects of treatment’’ to improve ‘‘community-hospital’’ patients’ management coordination. It is therefore natural that pharmacists were offered to be major players in the management of VTE in Champagne-Ardenne region. As a prerequisite and to update their knowledge, it seemed useful to make an a According to the HPST law, patient therapeutic education (PTE) aims to help patients better manage their lives with a chronic illness. It is a continuous process, part of the patient’s management. Pharmacists contribute to this process with their expertise as drug professionals; they can bring, with the other actors, autonomy to patients regarding their treatment (e.g. auto-injection for LMWH).

inventory of practices and knowledge of VTE and cancer. Thus, the primary endpoint of this study was to describe the organization, practices, and knowledge of pharmacists regarding management of VTE in cancer patients.

Materials and methods A working group set up this study. It brought together members of the Regional Union of Health Professionals ‘‘pharmacists’’ (Union Re´gionale des Professionnels de Sante´, Pharmaciens—URPSPharmaciens), Champagne-Ardenne Regional Cancer Network ONCOCHA, Faculties of Medicine and Pharmacy of Reims, Reims University Hospital, Institut Jean Godinot (Reims Regional Cancer Treatment Center), Actions Croise´es Association (association to support cancer patients), and the Regional Health Agency (Agence Re´gionale de Sante´—ARS) Champagne-Ardenne. The group received the institutional support of a pharmaceutical company, LEO Pharma.

Study type—sample This study was an electronic descriptive survey carried out among Champagne-Ardenne community pharmacists. A web-questionnaire was sent by email to all active community pharmacists (n ¼ 567) of the region by URPS-Pharmaciens.

Questionnaire An email explaining the process and including an Internet link to a questionnaire prepared using GoogleÕ DriveÕ was sent every week since 12 October 2013 until 15 November 2013. This survey was unpaid. The full questionnaire is available from the authors. The questionnaire was conducted with multiple choice or open questions and space for open comments. The questionnaire included 20 questions that addressed five aspects; pharmacists were asked to estimate the data if not available. 1. Location and practice mode (4 questions). 2. Pharmacy organization to support cancer patients (6 questions). Pharmacist dedicated to cancer issues? Pharmacist dedicated to supportive care? Implementation of pharmaceutical interviews? Staff trained in patients’ therapeutic education (PTE)? 3. Perception of the patient’s situation by the pharmacy team (4 questions). How is the pharmacist informed of the diagnosis of cancer? Estimated

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number of cancer patients among the pharmacy patients? Estimated number of patients with cancer and VTE among the pharmacy patients? Treatments prescribed for these cancer patients for VTE? 4. Guidelines and recommendations on the management of VTE in patients with cancer: understanding and practical application (4 questions). 5. Illustration by a simple case report (2 questions):  ‘‘In one of your patients, DVT was initially diagnosed and treated by a low-molecular weight heparin for one week. What, in your opinion, should be prescribed to continue this treatment?’’ The possible answers to this question were: Low-molecular weight heparins (which was the correct answer) g Fondaparinux g Anti-vitamin K g Direct Oral Anticoagulants (New Oral Anticoagulants) g Other (specify)  ‘‘What is, in your opinion, the recommended duration of treatment?’’ This was an open question. g

All questions expected an answer. Participants could only respond once to the questionnaire (IP address identification).

Statistical analysis A descriptive analysis was performed: quantitative variables were described by their mean (m), standard deviations (SD) and extreme values (minimum and maximum). Qualitative variables were described by the number of observations (n) and the corresponding percentage (%). Data were analyzed using SAS 9.0 (NC, Cary, USA).

Table 1. Characteristics of pharmacists. Characteristics Sex Male Female Age classes (years) 25–30 31–35 36–40 41–45 46–50 51–55 56–60 61–65 >66 Practice departmenta Ardennes Aube Haute-Marne Marne Practice location Urban Sub-urban Rural

n (%) 89 (49.7) 90 (50.3) 8 34 19 24 23 32 26 11 2

(4.5) (19.0) (10.6) (13.4) (12.9) (17.9) (14.5) (6.1) (1.1)

45 39 15 80

(25.1) (21.8) (8.4) (44.7)

61 (34.1) 36 (20.1) 82 (45.8)

a Champagne-Ardenne region is composed of four departments: Marne, Haute-Marne, Ardennes, and Aube.

The average number of pharmacists per pharmacy was 2.3 (SD ¼ 0.8; 1–5). The average number of pharmacy technicians per pharmacy was 2.4 (SD ¼ 1.3; 0–6). In the vast majority of pharmacies, (92.7%, n ¼ 166), no staff was dedicated to oncology. Pharmaceutical interview was set up in about one-third of pharmacies (36.9%, n ¼ 66). Finally, 9 pharmacies (5%) had at least one person trained in PTE, 12 pharmacies (6.7%) had developed a PTE project.

Patients with cancer and VTE Results The participation rate was 31.6% (n ¼ 179/567).

Description of the sample and organization of pharmacies Participation was similar between women and men. The average age was 46 years (SD ¼ 10.5 years). Pharmacists of the Marne were the most likely to respond; they represented about 45% of respondents (n ¼ 80/179). Pharmacists installed in rural areas were also more likely to respond (45.8%, n ¼ 80/179). The results are shown in Table 1.

The pharmacists were aware of the diagnosis of cancer most often by the patient or his relatives (n ¼ 164) or by interpretation of the prescriptions (n ¼ 121). Five pharmacists were informed by the oncologist and six by the general practitioner, and none was informed by the hospital pharmacist. The average number (estimated by the responding pharmacists) of patients with cancer estimated by pharmacies was 11.7 (SD ¼ 6.2, 3–25), and the average number of patients with cancer and VTE estimated by pharmacies was 4.1 (SD ¼ 3.8, 0–13). According to the pharmacists’ point of view and perception, LMWH were often dispensed to treat

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VTE in patients with cancer (n ¼ 131, 49% responded that they dispensed LMWH in cancer patients). However, many therapeutic classes were provided to patients (Figure 1).

these mostly on the Internet (INCA, http://www. thrombose-cancer.com, ANSM, AFSOS websites). Regarding the case report, the correct answer (according to recommendations) was LMWH for 3–6 months or as long as the cancer is active. The majority of pharmacists (49%, n ¼ 88) cited good therapeutic class (Figure 2). In contrast, only 25 pharmacists (14%) reported good treatment duration (other responses ranged from ‘‘10 days’’ to ‘‘life-long’’). Finally, 87 pharmacists responded the question regarding their needs for care of these patients.

Good clinical practice guidelines on the management of VTE in patients with cancer Eight pharmacists (4.5%) reported knowing the existence of recommendations on the management of VTE in patients with cancer. They stated that they found

Anlpatelet

8 (3%)

DOA

24 (9%)

Calcic heparin

12 (5%)

Fondaparinux

37 (14%)

AVK

54 (20%)

LMWH

131 (49%) 0

20

40

60

80

100

120

140

Figure 1. Venous thromboembolic disease treatments dispensed by pharmacists (estimated by responding pharmacists). DOA: direct oral anti-coagulants; AVK: anti-vitamin K; LMWH: low-molecular weight heparin.

10, 6%

10, 6%

88, 49%

70, 39%

LMWH

AVK

Fondaparinux

DOA

Figure 2. Answers to the question: ‘‘What treatment should be prescribed after 10 days of LMWH in patients with cancer?’’ DOA: direct oral anti-coagulants; AVK: anti-vitamin K; LMWH: low-molecular weight heparin.

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The pharmacists’ needs include education and training and information leaflets for the patients. The responses to patients’ questions were grouped in categories: . The thromboembolic disease as a whole . Management of DVT or PE with anticoagulants, stockings, and so forth . Risk of recurrent thrombosis . Duration of treatment . Adverse effects . Drug–drug and drug–food interactions.

Discussion This practices study in the Champagne-Ardenne region conducted with community professionals has mobilized since the answer rate was 31.6%. This figure may be regarded as satisfactory to the extent that this is an unusual approach. It shows that the recommendations in the management of thrombosis in cancer patients is not optimal and can be improved. The community pharmacists’ population who responded to this study is representative of the general population of pharmacists in Champagne-Ardenne, in terms of sex and age. Concerning the organization of pharmacies, they meet the needs of the population without any particular orientation regarding cancer. The number of cancer patients continues to increase, but it only represents a small part of the pharmacies’ patients. However, this does not prejudge time required and availability of the pharmacy team for optimal management of this patient population and their families. In the region, many pharmacists have implemented pharmaceutical interviews (63%). The question we asked was not accurate: it is likely that given the recent implementation of pharmaceutical interviews of patients on oral anticoagulants, the answer does not give a clear view of the proportion of pharmaceutical interviews specifically dedicated to cancer patients at the pharmacy. As a reminder, in accordance with the decree of 4 May 2012, the interview should in particular: . Strengthen the pharmacist’s role of counseling, education, and prevention with patients . Promote the pharmacist’s expertise on drugs . Assess the knowledge of the patient’s treatment . Seek therapeutic patient adherence and help him to control his treatment . Evaluate eventual patient’s ownership of his therapy. Interviews set up by pharmacists cover either a part or all of these objectives. In contrast, the proportion of pharmacists who have acquired validated therapeutic

patient education (TPE) competence (40 h of theoretical education) is very low (5%). The study shows that in almost all cases (96%), the pharmacy team is aware of the diagnosis of cancer through the patient and his family or by deduction of the contents of the prescription. Indeed, as a primary care professional, the pharmacist is at the heart of the treatment dispensing, including targeted therapies and supportive care. It is therefore essential to create a quick information link adapted from the hospital prescriber to the pharmacy team to ensure good continuity and safety of outpatient care. The thromboembolic risk is part of this management. It is linked to the disease progression and the administered treatment. National recommendations remind terms of good practice to treat VTE. At the community pharmacy level, the proportion of cancer patients with a risk of thromboembolism or proved thrombotic episode is high (approximately one-third of the active patients with cancer). A good knowledge of the latest recommendations is required. The study shows that the level of information on the existence of dedicated national or international recommendations is very low or nonexistent. Nearly one half of the questioned pharmacists recommended dispensing LMWH after the first days of treatment in accordance with these recommendations without knowing precisely the optimal duration of treatment. Spreading recommendations to pharmacists, as it has been done for physicians, should be a priority. It has been put in evidence that recommendations, when disseminated, are not applied by physicians,16 explaining that some patients were prescribed DOA or antiplatelet therapy. If pharmacists had had a good knowledge of recommendations, they could have made an intervention, calling the physician and having the prescription changed. Education and information are necessary, not to say compulsory; education and training sessions have been put in place in Champagne-Ardenne region. Sessions included the intricacies of cancer and VTE, on the one hand, and the different recommended and nonrecommended therapeutic options, on the other. Another questionnaire will be carried out by the end of 2014, to assess the impact of these sessions on pharmacists’ knowledge. Besides, e-learning projects could be launched to allow pharmacists (and physicians) to carry on with continuous education. Lastly, patients’ information leaflet was developed, explaining VTE and its treatment in a simple ‘‘patients’ language’’? This booklet has been validated by a patients’ association. Since 2002, cancer care has largely structured around care institutions by strengthening inter-relationships for better care of patients and caregivers. To ensure

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efficient care pathways, it is important that information is disseminated to all healthcare professionals involved in the care of patients. The dispensary pharmacist is at the forefront following the release of oral chemotherapies in community pharmacies. It also appears significant, with respect to the patient, to share between all health professionals (‘‘diagnosis and disease professionals,’’ i.e. physicians—oncologists and general practitioners, ‘‘drugs and therapeutics professionals,’’ i.e. hospital and community pharmacists, and ‘‘care professionals,’’ i.e. nurses) the same vision regarding treatments to optimize the proper monitoring of these and generate less stress in these cancer patients.

Conclusion There is no literature available on this subject, so it is difficult to compare our results with those of other studies of this type. A national questionnaire extended to all French regions is currently proposed to validate these results. In the region, the strategy of the working group is to meet the pharmacists’ needs in organizing departmental (one per department) education and training sessions and creating practical tools for the community pharmacist and for patients. Finally, a further questionnaire (with the same questions) will be issued using the same method at the end of 2014, to put in evidence if education and training improves knowledge and management, with the aim of ensuring a better overall patient care, in close link with every health professional. Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest All authors but Jean-Luc Ducrocq (i.e. Jean-Baptiste Rey, Nicolas Jovenin, Pierre Kreit, Je´roˆme Sicard, Damien Parent, Dominique Hettler, and Philippe Nguyen) have had a Consultant role with Leo Pharma. Jean-Luc Ducrocq is an employee of Leo Pharma. Besides, the authors have full control of all primary data and agree to allow the journal to review the data, if requested.

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Venous thromboembolism: What pharmacists know? What do they need?

Venous thromboembolism is common in cancer. Low-molecular weight heparins are recommended for prolonged treatment (3-6 months or more if the cancer is...
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