Specific author contributions: Richard Fedorak conceived and designed the study and edited the article. James Yeung created the data collection forms, performed the surveys, analyzed the data, and wrote the abstract and the article. Karen Goodman, a member of the Division of Gastroenterology and School of Public Health, contributed input to the questionnaire design and analysis and reviewed drafts of the article.
Article first published online: 18 FEB 2011
Copyright © 2011 Crohn's & Crohn's & Colitis Foundation of America, Inc.
Inflammatory Bowel Diseases
Volume 18, Issue 1, pages 34–40, January 2012
How to Cite
Yeung, J. H., Goodman, K. J. and Fedorak, R. N. (2012), Inadequate knowledge of immunization guidelines: A missed opportunity for preventing infection in immunocompromised IBD patients. Inflamm Bowel Dis, 18: 34–40. doi: 10.1002/ibd.21668
Funded through grants from the Crohn's and Colitis Foundation of Canada and the Centre of Excellence for Gastrointestinal Inflammation and Immunity Research.
- Issue published online: 11 DEC 2011
- Article first published online: 18 FEB 2011
- Manuscript Accepted: 6 JAN 2011
- Manuscript Received: 30 SEP 2010
- Crohn's disease;
- ulcerative colitis;
Immunosuppressive agents, used commonly to treat inflammatory bowel disease (IBD), are associated with an increased risk of infections, including those preventable by immunization. This study aimed to describe physician and patient values and knowledge regarding immunization and immunization histories.
In all, 167 IBD patients and 43 gastroenterologists completed mail-out questionnaires. Patients were asked 15 questions about their immunization histories and attitudes towards immunization. Gastroenterologists were asked nine questions about immunization for the immunocompromised host.
The questionnaire return rate was 45.7% (43/94) for gastroenterologists and 25.2% (167/661) for patients. Only 14.3% (6/42) of gastroenterologists reported taking an immunization history from most or all of their patients. Only 5.4% (9/167) of patients recalled being asked by their gastroenterologist whether their immunizations were up to date, and just 0.6% (1/164) recalled being asked for a detailed immunization history. Overall, 21.7% (35/161) of patients had refused to be immunized in the past; 18.6% (8/43) of gastroenterologists did not know if up-to-date immunizations were important prior to starting immunosuppressive therapy. Of note, 23.1% (9/39) of gastroenterologists and 46.7% (35/161) of patients did not know whether live vaccines should be avoided by those in the immunosuppressed state, and 42.9% (18/43) of gastroenterologists acknowledged they did not know which specific immunizations should be avoided for immunosuppressed patients.
Gastroenterologists have limited knowledge of their IBD patients' immunization status and rarely take an adequate immunization history. Substantial proportions of IBD patients and gastroenterologists lack adequate knowledge of established immunization guidelines prior to initiation of immunosuppressive therapy. (Inflamm Bowel Dis 2011;)
Inflammatory bowel disease (IBD) is a chronic inflammatory condition arising from an abnormal immunological response to bowel flora following from a complex interaction between environmental and microbial factors within the intestine.1 Treatment of IBD often requires suppression of the immune response using corticosteroids, antimetabolites (6-mercaptopurine [6-MP], azathioprine), methotrexate, and, more recently, biologic therapy. Such treatments place patients at increased risk of acquiring infections, many of which are potentially preventable through vaccination.2–8
The Public Health Agency of Canada (PHAC) offers well-established immunization guidelines for immunocompromised individuals. PHAC recommends that these individuals update all childhood immunizations (at diagnosis: diphtheria, tetanus, inactivated polio virus, acellular pertussis, hemophilus influenza type b, measles, mumps, rubella, and varicella) and obtain influenza (annually), tetanus (every 10 years), and pneumococcal (at diagnosis and a booster at 3–5 years) immunizations.9 A USA expert consensus report provided similar guidelines for immunizations for patients with IBD, with the alternate suggestion that, at diagnosis, adults without a clear history of chickenpox should have serological testing for varicella, and those whose tests do not show immunity should receive the varicella vaccine.10 There is no clear evidence that any of these immunizations would make a patient's IBD worse.
The PHAC also provides recommendations regarding the timing of these immunizations. The inappropriate use of live vaccines in immunocompromised hosts can result in serious adverse reactions including the uncontrolled replication of the virus or bacterium.9 The recommendation is that, ideally, all vaccines be administered 14 days before the initiation of immunosuppressive therapy, and, if it is impossible to do so, vaccination should take place 3 months after immunosuppressive agents have been stopped. This timeline applies for the administration of both inactivated and component vaccines (to maximize immunogenicity) and for live vaccines (to reduce risk of dissemination).9 In particular, the varicella, mumps, measles, and rubella vaccines only have a live option.
In terms of safety, Sands et al10 recommend that live vaccines be avoided by adults who have received prednisone (≥20 mg/d equivalent) for 2 weeks or more and within 3 months of stopping; those who have received 6-MP, methotrexate, or infliximab within the past 3 months; and patients who have significant protein-calorie malnutrition.
Despite these very clear guidelines, studies have shown that a significant number of patients with IBD remain inadequately immunized. For instance, Melmed et al11 studied 146 IBD patients who were on immunosuppressive medications for IBD and thus at increased risk of influenza and pneumococcal disease. Only 28.1% (41/146) had received the influenza vaccine, and 8.9% (13/146) had received the pneumococcal vaccine. The most common explanation patients gave was that they were “not aware of [the] need” for immunizations. Similar results were seen for varicella, tetanus, and hepatitis B virus (HBV) immunizations.
In light of the known risk of infection and the reported low rates of immunization for immunosuppressed IBD patients, we sought to investigate and describe knowledge and values regarding immunization among IBD patients and gastroenterologists.
MATERIALS AND METHODS
Study Site and Participants
The study was conducted at the Zeidler Gastroenterology Health Centre at the University of Alberta Hospital (Edmonton, Canada). The study consisted of similar surveys of two groups of subjects: a group drawn from the source pool of gastroenterologists practicing in the Province of Alberta and a group composed of IBD patients being treated by these gastroenterologists.
We used an electronic health record database to obtain a computer-generated list of IBD patients. All patients diagnosed with Crohn's disease (CD) or ulcerative colitis (UC), consecutively seen in follow-up consultation between 2005 and 2009, and over the age of 18 were invited to participate.
A packet that included a self-administered patient questionnaire, an information sheet regarding the study, and a stamped, addressed envelope was sent to each patient's mailing address. Patients were given 3 months to complete and return the questionnaire. Gastroenterologists, all members of the Alberta Society of Gastroenterology, were either given a self-administered questionnaire, an information sheet, and a stamped, addressed envelope in person at a local Alberta Society of Gastroenterology meeting (June 2009) or mailed these items.
Physicians were asked 15 questions in four general categories: 1) how frequently they took an immunization history from their IBD patients, and how frequently they would ask about individual immunizations; 2) what their overall opinions were toward immunizations, and the importance and safety of their use among IBD patients; 3) whether they thought their IBD patients had enough information about immunizations; and 4) whether immunizations were important and/or safe when starting their IBD patients on immunomodulators or anti-tumor necrosis factor (TNF) agents.
Patients were asked nine questions in five general categories: 1) how well they knew their own immunization histories, and any challenges they faced in keeping this knowledge; 2) how frequently their gastroenterologist had asked them a general or specific immunization history; 3) why certain patients refused immunizations before; 4) what their opinions were toward immunizations; and 5) what type of sources of information patients used to learn about immunizations.
Analysis of the results was completed and summaries of the answers are shown in the Results section. In circumstances where a question was left unanswered, the answer was considered missing for that one question, and the denominator for that question was reduced correspondingly to arrive at the proportion that gave a particular response out of all respondents who answered that question.
The Health Research Ethics Board (HREB) of the University of Alberta approved this study. Patients were given an information sheet regarding this research study. Patients were made aware that participation in this study was strictly voluntary, and that consent was implied in the overt action of the completion and submission of the questionnaire. Neither patients nor physicians were given any material or financial incentives for participating in this study. Returned surveys did not include any patient identifying information.
Ninety-four questionnaires were given or mailed to physicians, and 43 (45.7%, 43/94) of these physicians returned a completed questionnaire. The physicians who participated in this study had an average of 17.4 years of practice experience, and 39.5% (17/43) had more than 15 years of experience since completing gastroenterology training. In all, 72.1% (31/43) were males. Of the whole group of physician respondents, 60.4% (26/43) saw fewer than 50 new IBD patients each year, while 71.4% (30/42) saw more than 50 follow-up IBD patients each year. For complete physician characteristics, please refer to Table 1.
|Number of years since completion of GI training||43|
|How many new patients with IBD do you see each year?||42|
|How many follow-up patients with IBD do you see each year?||42|
|The dominant type of clinical practice you have is:||39|
|Gastroenterology and Hepatology||41.0||16|
|Type of IBD||167|
|How many years ago were you diagnosed with IBD?||159|
Most physicians rarely or never (69.0%, 29/42) took an immunization history from their IBD patients. Only 14.3% (6/42) of physicians reported taking immunization histories from most or all of their patients. A majority of the physicians (62.5%; 25/40) asked their IBD patients if their immunizations were up to date; however, 57.5% (23/40) did not ask for details about individual immunizations. The majority (>50%) of gastroenterologists did not inquire about individual immunizations for varicella, rubella, diphtheria, mumps, meningococcal, measles, polio, pneumococcal, hemophilus influenza type b, tetanus, or pertussis (Fig. 1). Furthermore, just 48.8% (20/41) asked at least half of their IBD patients whether they had had an influenza vaccine and only 42.5% (17/40) of the physicians asked at least half of their IBD patients whether they had received the hepatitis B vaccine.
Opinions Toward Immunizations
High proportions of gastroenterologists strongly or somewhat agreed that childhood immunizations are important for their IBD patients (80.5%, 33/41), that they are safe for their IBD patients (87.8%, 36/41), and that their IBD patients need to ensure that their immunizations are up to date (85.4%, 35/41). Similarly, 85.4% (35/41) of gastroenterologists strongly or somewhat agreed that they did not believe that alternative medicine could eliminate the need for immunizations for IBD patients. However, 31.7% (13/41) did not know whether (or which) immunizations could make their patients' IBD worse.
Gastroenterologists held divided opinions in response to several statements. Over a third of physicians, 39.0% (16/41), strongly or somewhat agreed that they were concerned about the potential side effects of immunizations on IBD patients, but 43.9% (18/41) were not. While 42.5% (17/40) of physicians strongly or somewhat agreed that live vaccines could give IBD patients serious cases of the diseases they were meant to prevent, 42.5% (17/40) thought they would not. Similarly, 41.0% (16/39) of gastroenterologists strongly or somewhat agreed that IBD patients should avoid all live vaccines, while 35.9% (14/39) thought they did not need to avoid live vaccines at all. An additional 23.1% (9/39) did not know whether live vaccines should be avoided or not.
For 13 specific immunizations (diphtheria, pertussis, polio, hemophilus influenza type b, varicella, measles, mumps, rubella, hepatitis B, influenza, meningococcus, pneumococcus, and tetanus), the proportion of gastroenterologists who considered each to be somewhat or very important ranged from 55.0% (22/40) for diphtheria to 80% (32/40) for influenza. Of note is the fact that 17.5% (7/40) and 15.0% (6/40) of gastroenterologists did not think it was very or at all important to immunize against diphtheria and tetanus, respectively. Also, 5.0% (2/40) of gastroenterologists thought it was not at all important for IBD patients to be immunized against influenza. Between 12.5% (5/40) and 28.2% (11/39) of gastroenterologists checked the “don't know” option when asked whether each of the 13 listed immunizations were important for their IBD patients.
Of the 13 specific immunizations listed above, there were only four that some gastroenterologists indicated that they were very or somewhat concerned about their safety in an immunocompromised IBD patient: varicella (32.5%, 13/40), measles (22.5%, 9/40), mumps (20.5%, 8/39), and rubella (20.0%, 8/40). These are the live vaccines that physicians were likely hesitant to administer for the immunocompromised host. Of the remaining nine immunizations, most gastroenterologists were not concerned about the safety effects, with the proportion of those indicating somewhat unconcerned or not at all concerned ranging from 55.3% (21/38) for polio to 75.0% (30/40) for hepatitis B and influenza. The proportion of those who checked the “don't know” option for their degree of concern about the safety of the immunizations being given to IBD patients ranged from 20.0%–38.5% (8/40 to 15/39).
Information About Immunizations
None of the 43 gastroenterologists thought their IBD patients had enough information about immunizations.
Immunizations in the Immunocompromised IBD Patient
A little over 40% of gastroenterologists felt that it was important for their IBD patients to be immunized with hepatitis B (44.2%, 19/43) and pneumococcus (41.9%, 18/43) vaccines before starting on immunomodulators and/or anti-TNF agents. Of the remaining 11 vaccines, between 25.6% (11/43) and 34.9% (15/43) of gastroenterologists thought it was important to be up to date for diphtheria, pertussis, polio, hemophilus influenza type b, varicella, rubella, influenza, meningococcus, and tetanus immunizations before starting immunosuppressive therapy. Overall, 18.6% (8/43) of gastroenterologists did not know whether it was important for their IBD patients to be up to date on any of their immunizations before starting immunomodulators and/or anti-TNF agents.
Roughly 20%–25% of gastroenterologists thought that measles (23.3%, 10/43), mumps (18.6%, 8/43), rubella (18.6%, 8/43), and varicella (25.6%, 11/43) should be avoided in the case of patients started on immunomodulators or anti-TNF agents. A large proportion, 41.9% (18/43), acknowledged that they did not know which vaccinations should be avoided when starting patients on immunomodulators and/or anti-TNF agents (Fig. 2).
A total of 661 questionnaires were mailed to patients and 167 (25.2%, 167/661) were returned completed. The average age for the patient group was 46.5 (18.4–81.4) years and 61.1% (102/167) were female. Most of this group had CD (59.3%, 99/167), while 40.1% (67/167) suffered from UC. On average, these patients had been diagnosed with IBD ≈14 (0.3–41) years ago. For complete patient characteristics, please refer to Table 1.
Personal Immunization Knowledge
Most patients thought they had received the following immunizations as a child [bracketed dates show when each vaccine was introduced in Canada]: diphtheria  (63.2%, 96/152), tetanus  (78.6%, 121/154), polio  (73.2%, 115/157), measles  (65.3%, 98/150), mumps  (61.6%, 93/151), and rubella  (53.0%, 79/149).9 Less than half the patients indicated that they had received pertussis [1940s] (43.2%, 64/148), hemophilus influenza type b  (19.0%, 27/142), and varicella  (17.0%, 24/141). Furthermore, of those who indicated that they had received specific immunizations, less than 40% actually knew the date of their last immunization, with the numbers ranging from 16.7% (4/24) for varicella to 37.5% (36/96) for diphtheria.
For immunizations administered in adults, the majority of patients knew they had received the influenza (62.2%, 92/148) or tetanus (71.1%, 106/149) vaccinations, and 44.7% (63/141) knew they had received the hepatitis B vaccination. However, only a small proportion of patients knew whether they had received meningococcal (8.8%, 12/136) or pneumococcal vaccinations (17.5%, 24/137).
However, less than 50% of patients thought they were up to date for influenza (47.6%, 50/105), hepatitis B (37.1%, 36/97), and tetanus (32.1%, 35/109). Only 4.2% (3/72) and 20.3% (16/79) thought they were up to date for meningococcal and pneumococcal vaccinations, respectively. Of those who claimed that their immunizations were up to date, the proportion of patients that knew the date of the last immunization ranged from 66.7% (2/3) for meningococcal vaccine to 94.0% (47/50) for influenza vaccine. Approximately half of the patients (51.5%, 86/167) thought they were either somewhat or completely up to date for their immunizations as recommended for their age, whereas the other 48.5% (81/167) did not know or thought they were not at all up to date.
More than a quarter, 26.3% (44/167), of the patients said that “misplaced immunization records” was the biggest challenge they faced in keeping their immunizations up to date. Other challenges included immunization records being kept at the doctor's office (23.4%, 39/167), patients having moved to a new city/province (19.8%, 33/167), and patients finding the information confusing (13.2%, 22/167). Many individuals selected “others” as the biggest challenge in keeping their immunizations up to date (31.7%, 53/167). For patients who chose “others,” the vast majority wrote in the space provided descriptions of challenges that were consistent with either a lack of awareness of specific immunizations or with a lack of understanding of their importance.
Only 5.4% (9/167) of patients reported being asked generally whether their immunizations were up-to-date, and only 0.6% (1/164) could recall being asked in detail for an immunization history.
Just over a fifth, 21.7% (35/161), of the patients said that they had refused to be immunized in the past. Of the individuals who stated they had refused an immunization in the past, 57.1% (20/35) had refused the influenza vaccination. Of those who had refused immunization in the past, 28.6% (10/35) had either been told by their doctors, read, or heard that it was not safe; 14.3% (5/35) claimed that their doctors told them that it was not necessary. Over half, 51.4% (18/35), also selected “other” reasons for why they had refused an immunization. Their written reasons included personal choice, concerns about side effects, and the belief that their bodies did not need to depend on immunizations to fight infections.
Opinions Toward Immunizations
The majority of patients somewhat or strongly agreed that routine immunizations are safe (82.3%, 135/164) and important for their health (81.8%, 135/165) and that they should ensure that all their immunizations are up to date (79.6%, 133/167). Most patients (69.7%, 115/165) somewhat or strongly disagreed that the use of alternative practices could eliminate the need for immunizations, although 22.4% (37/165) of the patients checked the “don't know” option for this statement. Conversely, 74.1% (123/166) of the patients did not know whether immunizations could make their IBD worse. Also, 58.4% (97/166) of patients strongly or somewhat agreed that they were concerned about the potential side effects of immunizations, 46.7% (77/165) did not know whether or not they should avoid live vaccines, and 68.1% (113/166) either did not know or somewhat or strongly disagreed that a live vaccine could give a serious case of the very same disease it was meant to prevent.
Most patients felt that each of the 13 specific immunizations (diphtheria, pertussis, polio, hemophilus influenza type b, varicella, measles, mumps, rubella, hepatitis B, influenza, meningococcus, pneumococcus, and tetanus) was important, with the proportion ranging from 43.8% (67/153) for varicella to 64.5% (100/155) for hepatitis B. Conversely, 15.4% (24/156) of the patients thought that the influenza vaccine was not important. Furthermore, sizable proportions of patients did not know how important specific immunizations were for them, ranging from 22.4% (35/156) for influenza to 44.1% (67/152) for hemophilus influenza type b.
Between 40.1% (65/162 for hemophilus influenza type b) and 50.3% (80/159 for influenza) of the patients were not concerned about the safety of any of the specified immunizations. There were no particular vaccines that patients were particularly concerned about in terms of safety. As well, between 18.2% (29/159 for influenza) and 30.1% (49/163 for diphtheria) of the patients did not know how concerned they were about the safety of specific immunizations.
Information About Immunizations
Patients were very confident in the immunization information provided by gastroenterologists (68.7%, 114/166) and family physicians (60.1%, 98/163); overall, most patients were at least somewhat or very confident in gastroenterologists (89.8%, 149/166), family doctors (93.3%, 152/163), the public health department (87.9% 145/165), nurses (85.5%, 141/165), pharmacists (86.3%, 139/161), hospitals (82.5%, 132/160), and books/journals (74.5%, 123/165). Patients were not very or at all confident in immunization information obtained from schools/daycares (43.3%, 71/164), chiropractors/naturopaths/alternative healthcare providers (46.0%, 74/161), family/friends (50.3%, 82/163), media (51.2%, 85/166), and the Internet (51.8%, 86/166).
Patients claimed that the largest source of immunization information came from family physicians (67.1%, 112/167). The public health department (51.5%, 86/167), media (44.3%, 74/167), and family/friends (43.1%, 72/167) were other major sources of information. Only 24.6% (41/167) of the patients indicated that their gastroenterologists were a source of immunization information for them.
Only 16.3% (27/166) of the patients thought they had enough information about immunizations. Two-thirds, 66.3% (110/166), indicated they did not have enough; while 17.5% (29/166) did not know. Nearly two-thirds, 65.5% (91/139), indicated they did not know they needed to be aware of the status of their immunizations, and 45.3% (63/139) noted that their gastroenterologist did not review this information with them.
In this study, gastroenterologists indicated they believed that childhood immunizations are important for IBD patients and that IBD patients need to ensure that their immunizations are up to date. IBD patients agreed with these statements. However, most gastroenterologists acknowledged rarely taking an immunization history from their IBD patients, and, when they did take immunization histories, most did not ask for details about specific immunizations. Similarly, very few patients recalled being asked if their immunizations were up to date and only one recalled being asked for a detailed immunization history. Expert consensus guidelines suggest that the complete immunization history should be reviewed before starting patients on immunosuppressive therapy.
None of the physicians felt that their IBD patients had enough information about immunizations, and most patients felt the same way. Paradoxically, the majority of patients indicated they were very confident in immunization information obtained from both gastroenterologists and family physicians, yet most of their immunization knowledge came from family physicians, with most patients indicating that they had had very little discussion of immunizations with their gastroenterologist. Ironically, the biggest challenges patients said they faced in keeping up to date with their immunizations were lack of awareness and misplaced immunization records. In fact, some patients indicated they had refused immunizations in the past, suggesting that they thought they would not benefit from an immunization or that it would do more harm than good. Practical solutions to this problem would include initiating a strategy for increasing awareness and creating a provincial or national database for immunization records.
With respect to immunizations commonly given in childhood, even among the patients who indicated that they had been immunized, less than 40% actually knew the date of their last immunization. Similarly, for immunizations that are often administered to adults, fewer than 50% of patients thought they were up to date on these specific immunizations and very few actually knew the date of their last immunization. This percentage suggests that although there is good recall among adults of their childhood and adult immunizations, most adults do not recall the details of immunization history. Many patients are not aware of the importance of immunizations that are newer or targeted to particular age or risk groups. Thus, the ability to obtain an accurate immunization history from adults may require that a complete immunization record be kept somewhere accessible.
A large proportion of gastroenterologists indicated that they did not know whether IBD patients should avoid live vaccines or not. In fact, a third of gastroenterologists did not know whether or not to avoid measles, mumps, rubella, or varicella (the live vaccines) for the immunocompromised host. These knowledge deficits may explain why gastroenterologists avoid discussing immunizations with their patients and thus miss an opportunity to prevent infections in their immunocompromised IBD patients.
Nearly 20% of gastroenterologists did not know how important it was for their IBD patients to be up to date on specific immunizations before starting immunomodulators and/or anti-TNF agents. Furthermore, over 40% of gastroenterologists acknowledged that they did not know which vaccines should be avoided when starting patients on immunomodulators and/or anti-TNF agents. However, the Public Health Agency of Canada and USA policy makers recommend that all IBD patients be (or be brought) up to date on the 13 specified immunizations at least 14 days before initiation of such immunosuppressive therapy. These findings highlight an important lack of knowledge of the clinical guidelines, one that could potentially result in missed opportunities for preventing infection via vaccinations.
There are several limitations of this study that should be acknowledged, largely deriving from the goal of keeping the questionnaires simple and brief. One of the challenges was that some of the patients simply did not have access to immunizations, whether because they were not within the targeted population, or because the vaccinations were not yet introduced. Furthermore, some vaccinations are optional, and sometimes patients would rather forgo the vaccination if the disease (e.g. influenza) is mild-to-moderate in nature, rather than risk vaccination side effects. Attempting to ascertain all of the relevant information for determining whether respondents were candidates for particular vaccines would have greatly complicated and lengthened the questionnaire.
Another limitation of the study is that mailed-out questionnaires do not offer any assistance to respondents who might have trouble in understanding questions; it is possible that some respondents interpreted questions other than as intended. Furthermore, patients are not asked why they chose a particular response. Gastroenterologists may have thought that the answers to some questions depended on the scenario (e.g., patient characteristics, on-going treatment plans) and thus they may have felt specific questions did not offer adequately nuanced choices; in particular, this may have contributed to “don't know” responses.
The response rate among patients is also low, which introduces some responder bias. However, such bias would be expected to shift findings toward greater knowledge among patients (assuming that more highly educated, knowledgeable patients are more likely to respond to surveys). In this setting, patients still demonstrated a striking lack of knowledge. Lastly, the study represents patients that are drawn from one institution whose practice patterns may not represent the larger community.
Overall, there needs to be a paradigm shift in the initial care of IBD patients, who are likely to become immunocompromised hosts in response to their IBD treatments. The results of this survey demonstrate the need for greater knowledge among both physicians and patients about immunization guidelines, specifically in terms of these immunizations' importance, safety, timing, and risks in relation to immunosuppressive therapy.
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- 11Patients with inflammatory bowel disease are at risk for vaccine-preventable illnesses. Am J Gastroenterol. 2006; 101: 1834–1840., , , et al.Direct Link: