Background Abdominal surgical site infections are among the most common complications of inpatient admissions and have serious consequences for outcomes and costs. Different risk factors may be involved, including age, sex, nutrition and immunity, prophylactic antibiotics, operation type and duration, type of shaving, and secondary infections. This study aimed to determine the risk factors affecting abdominal surgical site infections and their incidence at Imam Khomeini, a major referral teaching hospital in Iran.
Background
Abdominal surgical site infections are among the most common complications of inpatient admissions and have serious consequences for outcomes and costs. Different risk factors may be involved, including age, sex, nutrition and immunity, prophylactic antibiotics, operation type and duration, type of shaving, and secondary infections. This study aimed to determine the risk factors affecting abdominal surgical site infections and their incidence at Imam Khomeini, a major referral teaching hospital in Iran.Methods Patients (n = 802) who had undergone abdominal surgery were studied and the relationships among variables were analyzed by Student's t and Chi-square tests. The subjects were followed for 30 days and by a 20-item questionnaire. Data were collected through pre- and post-operative examinations and telephone follow-ups.
Methods
Patients (n = 802) who had undergone abdominal surgery were studied and the relationships among variables were analyzed by Student's t and Chi-square tests. The subjects were followed for 30 days and by a 20-item questionnaire. Data were collected through pre- and post-operative examinations and telephone follow-ups.Results Of the 802 patients, 139 suffered from SSI (17.4%). In 40.8% of the cases, the wound was dirty infected. The average age for the patients was 46.7 years. The operations were elective in 75.7% of the cases and 24.7% were urgent. The average duration of the operation was 2.24 hours, the average duration of pre-operative hospital stay 4.31 days and the average length of (pre- and post-operation) hospital stay 11.2 days. Three quarters of the cases were shaved 12 hours before the operation. The increased operation time, increased bed stay, electivity of the operation, septicity of the wound, type of incision, the administration of prophylactic antibiotic, type of operation, background disease, and the increased time lapse between shaving and operation all significantly associated with SSI with a p-value less than 0.001.
Results
Of the 802 patients, 139 suffered from SSI (17.4%). In 40.8% of the cases, the wound was dirty infected. The average age for the patients was 46.7 years. The operations were elective in 75.7% of the cases and 24.7% were urgent. The average duration of the operation was 2.24 hours, the average duration of pre-operative hospital stay 4.31 days and the average length of (pre- and post-operation) hospital stay 11.2 days. Three quarters of the cases were shaved 12 hours before the operation. The increased operation time, increased bed stay, electivity of the operation, septicity of the wound, type of incision, the administration of prophylactic antibiotic, type of operation, background disease, and the increased time lapse between shaving and operation all significantly associated with SSI with a p-value less than 0.001.Conclusion In view of the high rate of SSI reported here (17.4% compared with the 14% quoted in literature), this study suggests that by reducing the average operation time to less than 2 hours, the average preoperative stay to 4 days and the overall stay to less than 11 days, and approximating the timing of shaving to the operation and substituting cefazolin for cefaluthin when prophylactic antibiotic is to be administered, the SSI may be reduced to a more acceptable level.
Conclusion
In view of the high rate of SSI reported here (17.4% compared with the 14% quoted in literature), this study suggests that by reducing the average operation time to less than 2 hours, the average preoperative stay to 4 days and the overall stay to less than 11 days, and approximating the timing of shaving to the operation and substituting cefazolin for cefaluthin when prophylactic antibiotic is to be administered, the SSI may be reduced to a more acceptable level.

Background SSIs are among the most common hospital acquired infections comprising 14–16 percent of inpatient infections[ 1 ]. SSI is a dangerous condition, a heavy burden on the patient and social health system[ 2 ]. Such infections lengthens bed stay for an average of seven days. Potential sources of infection are the patient (especially contamination by alimentary tract bacteria), hospital environment, food, other patients, staff, infected surgical instruments, dressings, and even drugs and injections [ 3 ]. The incedence of SSIs with regard to abdominal surgical sites and operating conditions is as follows: Clean wounds (1.5–3.7%); clean-contaminated wounds (3–4%); contaminated wounds (8.5%); dirty-infected wounds (28–40%); in laparoscopy (10%) umbilical hernia (2–5%); in the cancer of the colon without taking antimicrobial drugs (30–60%); or with antibiotic and proper intestine wash (10%); in colostomy (above 50%); in colon perforation (20%); in stomach cancer and surgery (20%); in hernionite (50%); in adult appendectomy (10–20%); in children's appendicitis (2–5%); in aged appendicitis and in pregnant women (10–50%); and in AIDS victims (above 50%); in liver abscess (20%); in hydatid cyst (2–5%); in acute and chronic cholecystectomy without stones (10%); in acute septic cholangitis (10–20%); in laparoscopic cholecystectomy (2–5%); and in splenectomy (2–5%) [ 4 ]. SSI is identified with redness, inflammation, heat, pain, a temperature of 38°C, and septic drainage from the surgical site during the 30 days following operation[ 4 ]. Several factors are to be taken into account for SSI, some of which are as follows: While we could not find any significant correlation between sex and SSI rate, age proved to be an important factor; the rate of wound infection for 15 to 24-year-old patients was only10% but increased significantly for those over 65 years of age. The extent of SSI was doubled for obese patients. The duration of surgical operation also proved to be a significant factor: only 3% of operations lasting 30 minutes or less led to infection, while for operations lasting more than 6 hours this rate leapt to 18%. SSI rate increased with longer durations of preoperative bed stay, but preoperative showers with a disinfecting soap such as chlorhexidine or Betadine decreased the cutaneous bacterial load. According to Kruise, the rate of infection was reduced to 1.3% among patients who showered with disinfecting soap containing hexachlorophene. In those who showered with ordinary soap the corresponding figure was 2.1%, and for patients who did not shower at all it increased to 2.3%. However, another study on 5536 subjects showed no decrease in SSI in patients who showered with chlorhexidine preoperatively; the rate was 4% [ 4 ]. Among other factors that delay wound healing or increase the infection rate are cigarette smoking, which increases the postoperative infection rate 5-fold, and the use of steroids, which delays wound healing and increases the infection rate by 9 percentage points from 7% to 16%. Aseptic surgical techniques are claimed to decrease the infection rate, though not to zero [ 3 ]. However, the administration of prophylactic antibiotics 30 to 60 minutes before surgery, decreases the incidence of SSI [ 4 - 10 ]. Obviously, remote infections increase SSI. Other contributing factors are the type of surgery and secondary infections. The object of this study was to assess SSI, and the incedence of the factors contributing to such infections at Imam Khomeini Hospital in Iran.
Background
SSIs are among the most common hospital acquired infections comprising 14–16 percent of inpatient infections[ 1 ]. SSI is a dangerous condition, a heavy burden on the patient and social health system[ 2 ]. Such infections lengthens bed stay for an average of seven days. Potential sources of infection are the patient (especially contamination by alimentary tract bacteria), hospital environment, food, other patients, staff, infected surgical instruments, dressings, and even drugs and injections [ 3 ]. The incedence of SSIs with regard to abdominal surgical sites and operating conditions is as follows:Clean wounds (1.5–3.7%); clean-contaminated wounds (3–4%); contaminated wounds (8.5%); dirty-infected wounds (28–40%); in laparoscopy (10%) umbilical hernia (2–5%); in the cancer of the colon without taking antimicrobial drugs (30–60%); or with antibiotic and proper intestine wash (10%); in colostomy (above 50%); in colon perforation (20%); in stomach cancer and surgery (20%); in hernionite (50%); in adult appendectomy (10–20%); in children's appendicitis (2–5%); in aged appendicitis and in pregnant women (10–50%); and in AIDS victims (above 50%); in liver abscess (20%); in hydatid cyst (2–5%); in acute and chronic cholecystectomy without stones (10%); in acute septic cholangitis (10–20%); in laparoscopic cholecystectomy (2–5%); and in splenectomy (2–5%) [ 4 ].SSI is identified with redness, inflammation, heat, pain, a temperature of 38°C, and septic drainage from the surgical site during the 30 days following operation[ 4 ]. Several factors are to be taken into account for SSI, some of which are as follows:While we could not find any significant correlation between sex and SSI rate, age proved to be an important factor; the rate of wound infection for 15 to 24-year-old patients was only10% but increased significantly for those over 65 years of age. The extent of SSI was doubled for obese patients. The duration of surgical operation also proved to be a significant factor: only 3% of operations lasting 30 minutes or less led to infection, while for operations lasting more than 6 hours this rate leapt to 18%. SSI rate increased with longer durations of preoperative bed stay, but preoperative showers with a disinfecting soap such as chlorhexidine or Betadine decreased the cutaneous bacterial load. According to Kruise, the rate of infection was reduced to 1.3% among patients who showered with disinfecting soap containing hexachlorophene. In those who showered with ordinary soap the corresponding figure was 2.1%, and for patients who did not shower at all it increased to 2.3%. However, another study on 5536 subjects showed no decrease in SSI in patients who showered with chlorhexidine preoperatively; the rate was 4% [ 4 ]. Among other factors that delay wound healing or increase the infection rate are cigarette smoking, which increases the postoperative infection rate 5-fold, and the use of steroids, which delays wound healing and increases the infection rate by 9 percentage points from 7% to 16%. Aseptic surgical techniques are claimed to decrease the infection rate, though not to zero [ 3 ]. However, the administration of prophylactic antibiotics 30 to 60 minutes before surgery, decreases the incidence of SSI [ 4 - 10 ]. Obviously, remote infections increase SSI. Other contributing factors are the type of surgery and secondary infections. The object of this study was to assess SSI, and the incedence of the factors contributing to such infections at Imam Khomeini Hospital in Iran.Methods In this study, 802 patients in a teaching hospital during the 15 months from April 2002 to July 2003 underwent abdominal surgery and were studied for SSI and the factors affecting it. Initially, 884 patients were recruited for the study but 82 were excluded on the basis of the following criteria: deficient medical records; patients operated at a different hospital and subsequently transferred to Imam's Hospital: or patients deceased during the operation or within the following 30 days. The dependent variable in this study was abdominal surgical site infection, defined as redness, swelling, pain, temperature above 38°C, during the 30 days after operation. The independent variables were: age, sex, site operated, body mass index, time of shaving the site of incision, administration of prophylactic antibiotics, type of surgical operation, duration of operation, duration of preoperative bed stay; preoperative shower, type of shaving, and accompanying conditions. The data were collected through a 20-item questionnaire. The stages for data collection and information completion were as follows: identification of patients; preoperative interview; postoperative interview; record completion; weekly examinations and telephone follow-ups for 30 days following operation; and pre-discharge examinations. The collected data were analyzed by the SPSS 10 package, using Student's t-test for continuous variables and chi-square test.for categorical variables. To the best of our ability, this study was conducted with due attention to research ethics.however, problems met in the follow-ups the patient's discharge imposed limitations on the study
Methods
In this study, 802 patients in a teaching hospital during the 15 months from April 2002 to July 2003 underwent abdominal surgery and were studied for SSI and the factors affecting it. Initially, 884 patients were recruited for the study but 82 were excluded on the basis of the following criteria: deficient medical records; patients operated at a different hospital and subsequently transferred to Imam's Hospital: or patients deceased during the operation or within the following 30 days.The dependent variable in this study was abdominal surgical site infection, defined as redness, swelling, pain, temperature above 38°C, during the 30 days after operation. The independent variables were: age, sex, site operated, body mass index, time of shaving the site of incision, administration of prophylactic antibiotics, type of surgical operation, duration of operation, duration of preoperative bed stay; preoperative shower, type of shaving, and accompanying conditions.The data were collected through a 20-item questionnaire. The stages for data collection and information completion were as follows: identification of patients; preoperative interview; postoperative interview; record completion; weekly examinations and telephone follow-ups for 30 days following operation; and pre-discharge examinations. The collected data were analyzed by the SPSS 10 package, using Student's t-test for continuous variables and chi-square test.for categorical variables.To the best of our ability, this study was conducted with due attention to research ethics.however, problems met in the follow-ups the patient's discharge imposed limitations on the studyResults Of the 802 patients studied who had undergone abdominal surgery 139 (17.4%) suffered from SSI as defined in Table  1 . No infections were observed in the other 663 cases (82.7%). So far as wound type was concerned, we found clean wounds in 109 cases (13.6%); clean-contaminated wounds in 214 cases (26.7%); contaminated wounds in 307 cases (45.8%); and dirty infected wounds in 112 cases (14%). While 255 cases (28.1%) did not shower before the operation, the other 577 patients (71.9%) did. Table 1 Population Distribution based on the type of operation and SSI Incidence. Type of operation Frequency Percent SSI incidence Percent splenectomy 24 3 -- -- cholecystectomy 272 33.9 25 9.2 umbilical hernia 35 4.4 5 14.3 appendicitis 132 16.5 19 14.4 stomach cancer 58 7.2 23 39.7 Excision biopsy 15 1.9 -- -- laparotomy 142 17.7 25 17.6 cystectomy 9 1.1 4 44.4 colon cancer 24 3 14 58.3 colostomy 15 1.9 10 66.7 laparoscopy 18 2.2 -- -- abdominal mass 10 1.2 2 20 ileostomy 10 1.2 5 50 Intestinal adhesion 5 0.6 4 80 others 33 4.2 4 12.1 total 802 100 140 17.4 The body mass index for 73 patients (9.1%) was above 30, indicating obesity. Over half the patients (403 cases) suffered from accompanying conditions such as diabetes, high arterial blood pressure, kidney or liver failure, malignancy, febrile condition, cardiac disorders, thyroid disorders, blood disease, chronic obstructive pulmonary disease, convulsion, hyperlipidemia, or immunological disorders; or had previously undergone surgical operations. The rest were free of accompanying conditions (Table  2 ). Table 2 SSI Distribution based on the factors involved. Variable Classification SSI (+) SSI (-) total P. Val. N % N % N % Age Age groups under 25 4 3.7 103 96.3 107 100 <0.001 Age groups 25–65 102 18.1 462 81.9 564 100 Age groups above 65 33 25.2 98 74.8 131 100 Sex Female 61 15.1 344 84.9 405 100 <0.093 male 78 19.6 319 80.4 397 100 Type Of Wounds Clean wounds 5 4.6 104 95.4 109 100 <0.001 Clean contaminated wounds 9 4.2 205 95.8 214 100 Contaminated wounds 115 31.3 252 68.7 367 100 Dirty – infected wounds 10 8.9 102 91.1 112 100 Type Of Operation Urgent 29 14.9 166 85.1 195 100 <0.001 elective 110 18.1 497 81.9 607 100 Operation Duration Below 1.5 hours 9 5.4 157 94.6 166 100 <0.001 1.5 – 4 hours 121 19.5 501 80.5 622 100 Above 4 hours 9 64.3 5 35.7 14 100 preoperative bed stay Emergency 24 11.7 181 88.3 205 100 <0.018 1 – 15 days 100 18.6 439 81.4 539 100 More than 15 days 15 25.9 43 74.1 58 100 Shaving Time One hour before operation 29 14.5 171 85.5 200 100 <0.001 12 hours before operation 110 18.3 492 81.7 602 100 showering Before op. Taken 80 13.9 497 86.1 577 100 1.00 none 59 26.2 166 76.8 255 100 Body mass index Under 20 10 17.2 48 82.8 58 100 0.692 Ranging 20.1 – 25 73 16 383 84 456 100 Ranging 25.1 – 30 42 19.5 173 80.5 215 100 Above 30.1 14 19.2 59 80.8 73 100 We found no significant correlations between SSI incidence and sex or preoperative shower. However, correlations with duration of operation, duration of preoperative bed stay, electivity of surgery, lengthening of preoperative shaving time, increasing age, wound infection, site of surgery, type of incision, accompanying disorders, and type of prophylactic antibiotic administered before operation were all significant at p < 0.001. Although differences in SSI rates were not significantly related to BMI, a trend was apparent: SSI rate was higher with low and high BMI. The following prophylactic antibiotics were used: ampicillin, gentamicine, cephalothin, metronidazole, ceftriaxone and cefazoline (table  3 ). Table 3 SSI Distribution based on the type of prophylactic antibiotic administered. variables SSI cefazolin ceftriaxone Metronidazole cephalothin Gentimicine Ampicillin A NA A NA A NA A NA A NA A NA A N % N % N % N % N % N % N % N % N % N % N % N % positive 42 12.1 97 21.3 73 24.5 66 13.1 79 24 60 12.7 19 17 120 17.4 70 30.4 69 12.1 5 50 134 16.9 negative 305 87.9 358 78.7 225 75.5 438 86.9 250 76 413 87.3 93 83 570 82.6 160 69.6 503 87.9 5 50 658 83.1 total 347 100 455 100 298 100 504 100 329 100 473 100 112 100 690 100 230 100 572 100 10 100 792 100 P-Value P = 0.001 P < 0.001 P < 0.001 P = 1.000 P < 0.001 P = 0.018 A = applied NA = not applied
Results
Of the 802 patients studied who had undergone abdominal surgery 139 (17.4%) suffered from SSI as defined in Table  1 . No infections were observed in the other 663 cases (82.7%). So far as wound type was concerned, we found clean wounds in 109 cases (13.6%); clean-contaminated wounds in 214 cases (26.7%); contaminated wounds in 307 cases (45.8%); and dirty infected wounds in 112 cases (14%). While 255 cases (28.1%) did not shower before the operation, the other 577 patients (71.9%) did.Population Distribution based on the type of operation and SSI Incidence.Type of operationFrequencyPercentSSI incidencePercentThe body mass index for 73 patients (9.1%) was above 30, indicating obesity. Over half the patients (403 cases) suffered from accompanying conditions such as diabetes, high arterial blood pressure, kidney or liver failure, malignancy, febrile condition, cardiac disorders, thyroid disorders, blood disease, chronic obstructive pulmonary disease, convulsion, hyperlipidemia, or immunological disorders; or had previously undergone surgical operations. The rest were free of accompanying conditions (Table  2 ).SSI Distribution based on the factors involved.VariableClassificationSSI (+)SSI (-)totalP. Val.N%N%N%AgeAge groups under 25<0.001Age groups 25–65Age groups above 65SexFemale<0.093maleType Of WoundsClean wounds<0.001Clean contaminated woundsContaminated woundsDirty – infected woundsType Of OperationUrgent<0.001electiveOperation DurationBelow 1.5 hours<0.0011.5 – 4 hoursAbove 4 hourspreoperative bed stayEmergency<0.0181 – 15 daysMore than 15 daysShaving TimeOne hour before operation<0.00112 hours before operationshowering Before op.Taken1.00noneBody mass indexUnder 200.692Ranging 20.1 – 25Ranging 25.1 – 30Above 30.1We found no significant correlations between SSI incidence and sex or preoperative shower. However, correlations with duration of operation, duration of preoperative bed stay, electivity of surgery, lengthening of preoperative shaving time, increasing age, wound infection, site of surgery, type of incision, accompanying disorders, and type of prophylactic antibiotic administered before operation were all significant at p < 0.001. Although differences in SSI rates were not significantly related to BMI, a trend was apparent: SSI rate was higher with low and high BMI.The following prophylactic antibiotics were used: ampicillin, gentamicine, cephalothin, metronidazole, ceftriaxone and cefazoline (table  3 ).SSI Distribution based on the type of prophylactic antibiotic administered.A = appliedNA = not appliedDiscussion For the 802 participants in this study, the SSI reported was 17.4%, which is well above the 14–16% reported in other studies [ 1 ]. There were particularly high values in cases of umbilical hernia (14.3% compared with previously reported 5%) and stomach cancer (39.7%; in previous studies 20%) [ 4 ]. Increasing age is correlated with greater likelihood of certain chronic conditions, malnutrition and a fall in the body immunological efficiency, causing more extensive SSI [ 4 ]. The present findings supported this argument (p = 0.001). SSI is not correlated with sex [ 5 ], in agreement with previous findings (p = 0.093). The literature shows that SSI increases with obesity, one reason being a decrease in blood circulation in fat tissues [ 7 ]. Malnutrition is another factor predisposing to SSI [ 5 ]. In this study we considered a BMI of above 30 obese and that of below 20 as malnutrition, found no significant correlations between the two ranges and SSI extensity (p = 0.692). But, the previously reported correlation between SSI and pre-operation bed stay (p = 0.018) [ 4 , 5 ] was supported by this study. This is one of the factors to be taken into account. Thus by reducing pre-operation bed stay we may decrease SSI. The findings of this study also proved the risk of SSI to be less in elective surgeries than those referred to emergency departments as cases of acute abdomen, which could result from lack of readiness for operation on the patient's side. Here we should reduce risk factors by preparing the patient for the urgent operation as much as possible. The findings supported the literature by showing that administration of prophylactic antibiotic half an hour before the operation would bring about the best results and the lowest SSI [ 10 ]. This was proved for all antibiotics (p = 0.001) with the exception of cephalothin with (p = 1), which requires a lot more research. The literature shows that with the duration of above 2 hours, the risk of SSI increases [ 4 ]. The average time in this study was 2.24 hours, which must be reduced to below 2 hours although the nature of surgical operations is not always the same. The time of shaving when it approaches the operation and if done by clippers, reduces the SSI risk. In this study the two times: one hour before surgical operations and 12 hours before that were contrasted which supported previous findings with p = 0.001. This is one area where we can lower the risk by approximating the time of shaving as much as possible to that of operation. Other such factors quoted in the literature as the conditions of the operating theatre, personal hygiene, acompanying diseases, immunological disorders, smoking, techniques of surgery, the surgeon's expertise, duration of surgical scrub, preoperative skin preparation, poor hemostasis, failure to obliterate dead space, tissue trauma, and inadequate sterilization of instruments, which were not included in this study might be considered as confounding factors.
Discussion
For the 802 participants in this study, the SSI reported was 17.4%, which is well above the 14–16% reported in other studies [ 1 ]. There were particularly high values in cases of umbilical hernia (14.3% compared with previously reported 5%) and stomach cancer (39.7%; in previous studies 20%) [ 4 ]. Increasing age is correlated with greater likelihood of certain chronic conditions, malnutrition and a fall in the body immunological efficiency, causing more extensive SSI [ 4 ]. The present findings supported this argument (p = 0.001).SSI is not correlated with sex [ 5 ], in agreement with previous findings (p = 0.093). The literature shows that SSI increases with obesity, one reason being a decrease in blood circulation in fat tissues [ 7 ]. Malnutrition is another factor predisposing to SSI [ 5 ]. In this study we considered a BMI of above 30 obese and that of below 20 as malnutrition, found no significant correlations between the two ranges and SSI extensity (p = 0.692). But, the previously reported correlation between SSI and pre-operation bed stay (p = 0.018) [ 4 , 5 ] was supported by this study. This is one of the factors to be taken into account. Thus by reducing pre-operation bed stay we may decrease SSI. The findings of this study also proved the risk of SSI to be less in elective surgeries than those referred to emergency departments as cases of acute abdomen, which could result from lack of readiness for operation on the patient's side. Here we should reduce risk factors by preparing the patient for the urgent operation as much as possible.The findings supported the literature by showing that administration of prophylactic antibiotic half an hour before the operation would bring about the best results and the lowest SSI [ 10 ]. This was proved for all antibiotics (p = 0.001) with the exception of cephalothin with (p = 1), which requires a lot more research.The literature shows that with the duration of above 2 hours, the risk of SSI increases [ 4 ]. The average time in this study was 2.24 hours, which must be reduced to below 2 hours although the nature of surgical operations is not always the same.The time of shaving when it approaches the operation and if done by clippers, reduces the SSI risk. In this study the two times: one hour before surgical operations and 12 hours before that were contrasted which supported previous findings with p = 0.001. This is one area where we can lower the risk by approximating the time of shaving as much as possible to that of operation.Other such factors quoted in the literature as the conditions of the operating theatre, personal hygiene, acompanying diseases, immunological disorders, smoking, techniques of surgery, the surgeon's expertise, duration of surgical scrub, preoperative skin preparation, poor hemostasis, failure to obliterate dead space, tissue trauma, and inadequate sterilization of instruments, which were not included in this study might be considered as confounding factors.Conclusion Considering the relatively higher rate of SSI in this study (17.4% compared with the 14% quoted in the literature), especially in such cases as stomach cancers and umbilical hernia, where the rate is considerablly higher, we should carefully reconsider the whole operation procedure. In general, we should do our best to reduce the average operation duration to less than 2 hours and the average preoperative bed stay to less than 4 days. Thus, the present average of 11.2 days for the total bed stay would be reduced to less than 11 days. The time of shaving should approximate the operation time as much as possible. Finally, when the administration of prophylactic antibiotics is required, cefazoline is recommended to substitute cephalothin. Razavy: main researcher (design, analysis, report) Ibrahimpour: (implementation, analysis) Sabouri Kashani: (report, edit) Jafarian: (counsult)
Conclusion
Considering the relatively higher rate of SSI in this study (17.4% compared with the 14% quoted in the literature), especially in such cases as stomach cancers and umbilical hernia, where the rate is considerablly higher, we should carefully reconsider the whole operation procedure. In general, we should do our best to reduce the average operation duration to less than 2 hours and the average preoperative bed stay to less than 4 days. Thus, the present average of 11.2 days for the total bed stay would be reduced to less than 11 days. The time of shaving should approximate the operation time as much as possible. Finally, when the administration of prophylactic antibiotics is required, cefazoline is recommended to substitute cephalothin.Razavy: main researcher (design, analysis, report)Ibrahimpour: (implementation, analysis)Sabouri Kashani: (report, edit)Jafarian: (counsult)Competing interests The author(s) declare that they have no competing interests.
Competing interests
The author(s) declare that they have no competing interests.Pre-publication history The pre-publication history for this paper can be accessed here:
Pre-publication history
The pre-publication history for this paper can be accessed here:


Background Engaging practicing physicians in educational strategies that reinforce guideline adoption and improve the quality of healthcare may be difficult. Push technologies such as email offer new opportunities to engage physicians in online educational reinforcing strategies. The objectives are to investigate 1) the effectiveness of email announcements in engaging recruited community-based primary care physicians in an online guideline reinforcement strategy designed to promote Chlamydia screening, 2) the characteristics of physicians who respond to email announcements, as well as 3) how quickly and when they respond to email announcements.
Background
Engaging practicing physicians in educational strategies that reinforce guideline adoption and improve the quality of healthcare may be difficult. Push technologies such as email offer new opportunities to engage physicians in online educational reinforcing strategies. The objectives are to investigate 1) the effectiveness of email announcements in engaging recruited community-based primary care physicians in an online guideline reinforcement strategy designed to promote Chlamydia screening, 2) the characteristics of physicians who respond to email announcements, as well as 3) how quickly and when they respond to email announcements.Methods Over a 45-week period, 445 recruited physicians received up to 33 email contacts announcing and reminding them of an online women's health guideline reinforcing CME activity. Participation was defined as physician log-on at least once to the website. Data were analyzed to determine participation, to compare characteristics of participants with recruited physicians who did not participate, and to determine at what point and when participants logged on.
Methods
Over a 45-week period, 445 recruited physicians received up to 33 email contacts announcing and reminding them of an online women's health guideline reinforcing CME activity. Participation was defined as physician log-on at least once to the website. Data were analyzed to determine participation, to compare characteristics of participants with recruited physicians who did not participate, and to determine at what point and when participants logged on.Results Of 445 recruited physicians with accurate email addresses, 47.2% logged on and completed at least one module. There were no significant differences by age, race, or specialty between participants and non-participants. Female physicians, US medical graduates and MDs had higher participation rates than male physicians, international medical graduates and DOs. Physicians with higher baseline screening rates were significantly more likely to log on to the course. The first 10 emails were the most effective in engaging community-based physicians to complete the intervention. Physicians were more likely to log on in the afternoon and evening and on Monday or Thursday.
Results
Of 445 recruited physicians with accurate email addresses, 47.2% logged on and completed at least one module. There were no significant differences by age, race, or specialty between participants and non-participants. Female physicians, US medical graduates and MDs had higher participation rates than male physicians, international medical graduates and DOs. Physicians with higher baseline screening rates were significantly more likely to log on to the course. The first 10 emails were the most effective in engaging community-based physicians to complete the intervention. Physicians were more likely to log on in the afternoon and evening and on Monday or Thursday.Conclusions Email course reminders may enhance recruitment of physicians to interventions designed to reinforce guideline adoption; physicians' response to email reminders may vary by gender, degree, and country of medical training. Repetition of email communications contributes to physician online participation.
Conclusions
Email course reminders may enhance recruitment of physicians to interventions designed to reinforce guideline adoption; physicians' response to email reminders may vary by gender, degree, and country of medical training. Repetition of email communications contributes to physician online participation.

Background Many clinical practice guidelines have been disseminated through print publications and the Internet to improve the quality of healthcare. Complex physician behavior-change interventions have been created and applied to clinical practice guidelines to determine if the guidelines are being practiced. Research indicates that the adoption of clinical practice guidelines continues to lag behind their production and dissemination [ 1 ]. Adoption of such guidelines has been improved by the use of secondary strategies, which involve education, audit and feedback, benchmarking, office system interventions, and multifaceted interventions [ 1 ]. Continuing medical education (CME) providers and others interested in improving the quality of health care have had difficulty actively engaging practicing physicians in secondary strategies that may lead to guideline adoption [ 2 ], since CME courses and other educational interventions must compete with the physician learner's multiple priorities [ 3 ]. Over the past ten years, accessibility to educational opportunities has increased with advancements in technology, particularly the Internet. The Internet offers a delivery system for educational interventions and research activities that are more convenient to the physician learner than traditional live large group lectures and seminars [ 4 ]. The Internet generally functions in a passive manner, or as a "pull" technology, allowing the user to determine when, where and how to seek information. Engaging physicians in online educational activities may require the use of "push" technologies rather than pull technologies. "Push" technologies allow information to be delivered to the user rather than requiring the user to actively search for the desired in f ormation; they require minimal effort on the part of the recipient, which greatly supports their adoption [ 5 ]. Email was the first type of online push technology [ 5 ]. Other forms of push technologies are actively used such as pop-ups, list-serves, and screen savers. Based on preliminary research presented at the  Proceedings of the American Medical Informatics Association's 2002 Annual Symposium , screen savers have been shown to be effective as a reminder system in engaging physicians in bioterrorism CME activity, although the use of email has exceeded all other Internet applications [ 5 ]. Flanagan and colleagues demonstrated promise for email as a means of engaging physicians in online activities designed to reinforce guideline use. They found physician response rate to email solicitation to be 50% over a 14-month study period [ 6 ]. Beyond this, little is known about the effectiveness of email in engaging physicians in online educational interventions designed to improve the quality of healthcare [ 7 ]. The purposes of this study were to investigate 1) the effectiveness of email reminders in engaging recruited community-based primary care physicians in an online guideline reinforcement strategy that was designed to promote women's health, 2) the characteristics of physicians who respond to email announcements, as well as 3) how quickly and when they respond to email announcements.
Background
Many clinical practice guidelines have been disseminated through print publications and the Internet to improve the quality of healthcare. Complex physician behavior-change interventions have been created and applied to clinical practice guidelines to determine if the guidelines are being practiced. Research indicates that the adoption of clinical practice guidelines continues to lag behind their production and dissemination [ 1 ]. Adoption of such guidelines has been improved by the use of secondary strategies, which involve education, audit and feedback, benchmarking, office system interventions, and multifaceted interventions [ 1 ]. Continuing medical education (CME) providers and others interested in improving the quality of health care have had difficulty actively engaging practicing physicians in secondary strategies that may lead to guideline adoption [ 2 ], since CME courses and other educational interventions must compete with the physician learner's multiple priorities [ 3 ].Over the past ten years, accessibility to educational opportunities has increased with advancements in technology, particularly the Internet. The Internet offers a delivery system for educational interventions and research activities that are more convenient to the physician learner than traditional live large group lectures and seminars [ 4 ]. The Internet generally functions in a passive manner, or as a "pull" technology, allowing the user to determine when, where and how to seek information. Engaging physicians in online educational activities may require the use of "push" technologies rather than pull technologies. "Push" technologies allow information to be delivered to the user rather than requiring the user to actively search for the desired in f ormation; they require minimal effort on the part of the recipient, which greatly supports their adoption [ 5 ]. Email was the first type of online push technology [ 5 ]. Other forms of push technologies are actively used such as pop-ups, list-serves, and screen savers. Based on preliminary research presented at the  Proceedings of the American Medical Informatics Association's 2002 Annual Symposium , screen savers have been shown to be effective as a reminder system in engaging physicians in bioterrorism CME activity, although the use of email has exceeded all other Internet applications [ 5 ].Proceedings of the American Medical Informatics Association's 2002 Annual SymposiumProceedings of the American Medical Informatics Association's 2002 Annual SymposiumFlanagan and colleagues demonstrated promise for email as a means of engaging physicians in online activities designed to reinforce guideline use. They found physician response rate to email solicitation to be 50% over a 14-month study period [ 6 ]. Beyond this, little is known about the effectiveness of email in engaging physicians in online educational interventions designed to improve the quality of healthcare [ 7 ]. The purposes of this study were to investigate 1) the effectiveness of email reminders in engaging recruited community-based primary care physicians in an online guideline reinforcement strategy that was designed to promote women's health, 2) the characteristics of physicians who respond to email announcements, as well as 3) how quickly and when they respond to email announcements.Methods This study is a subanalysis of data from a randomized controlled trial (RCT), described in detail elsewhere [ 8 ]. The goal of the RCT was to improve Chlamydia screening rates of at-risk young women by community-based primary care physicians by using a multi-faceted online guideline reinforcement intervention. Primary care physicians were recruited from a national sample of 923 eligible offices identified by a large managed care organization's administrative data. Eligible offices had at least 20 young women (ages 16–26) at risk for chlamydial infection and at least one primary care physician (Internal Medicine, Family Medicine/General Practice, Pediatrics) with Internet access. In Phase I of recruitment occurred at the office level and Phase II at the physician level. In Phase I, all eligible offices were invited to participate via facsimile; an office was designated as "recruited" when one of its physicians declared intent to participate. In Phase II, an active link to the Intervention module was e-mailed to physicians recruited in Phase I. Recruited physicians were assigned at the time of logon to either a control or Internet CME intervention arm designed to improve Chlamydia screening rates; physicians within the same office were assigned to the same arm of the study. We designated physicians as "participating" when they first engaged the Internet intervention. The study was conducted between February 1, 2002 and December 31, 2002. The intervention included a series of four modules, feedback of performance data and a quality improvement toolbox. The education modules were based upon adult learning and behavior change theory [ 8 ]. Our driving principles included case-based learning [ 9 , 10 ] making programs interactive by adapting to the program learners' readiness-to-change stage [ 11 ] and performance feedback for behavioral motivation and reinforcement [ 12 ] The control condition was a series of four text-based modules on topics unrelated to Chlamydia. Physicians receive 1 category 1 CME credit per module for their participation. The main outcome measure was Chlamydia screening rates. The subanalysis of this trial focuses on the use of email reminders to engage physicians in the online intervention. Physician recruitment occurred from November of 2001 to January of 2002. Following recruitment, the intervention was initiated in February of 2002 via email broadcast to recruited physicians. During 2002, four separate educational modules were offered. Each module was introduced with a series of email announcements followed by email reminders that contained tailored subject line (i.e. Dear Dr. John Smith) and text message containing the URL that would connect the physician directly to the educational module. The first three modules, emphasized: (1) young sexually active women are at high risk for asymptomatic infection that may lead to future serious health consequences; (2) newer urine-based screening allows diagnosis without a pelvic examination; and (3) infection may be effectively treated with a one-dose antibiotic. The fourth module reviewed previously introduced concepts. A total of 33 announcements and reminders were sent to recruited physicians between February 1, 2002 and December 31, 2002, which represents one reminder overall for each 1.5 weeks of the study duration. Initially, we were concerned that frequent email reminders would be considered intrusive. After a trial period, we found that we could increase the frequency of reminders without difficulty, thus fewer email reminders were sent during the initial phases of the study. For the subanalysis of this trial, the principal outcome measure is participation, defined as physician log-on at least once to the website. Data was collected electronically when physicians logged on to the intervention. In addition, several evaluation questions were used at the conclusion of the online educational activities to explore CME preferences. Descriptive analyses of patient and physician demographics are used to compare baseline characteristics of patients and physicians in the email participants versus the recruited non-participants. Statistical significance is determined with tests appropriate to the distribution of the data (chi-square for categorical variables and student-t test for continuous variable). Two-tailed tests are used for all analyses.
Methods
This study is a subanalysis of data from a randomized controlled trial (RCT), described in detail elsewhere [ 8 ]. The goal of the RCT was to improve Chlamydia screening rates of at-risk young women by community-based primary care physicians by using a multi-faceted online guideline reinforcement intervention. Primary care physicians were recruited from a national sample of 923 eligible offices identified by a large managed care organization's administrative data. Eligible offices had at least 20 young women (ages 16–26) at risk for chlamydial infection and at least one primary care physician (Internal Medicine, Family Medicine/General Practice, Pediatrics) with Internet access. In Phase I of recruitment occurred at the office level and Phase II at the physician level. In Phase I, all eligible offices were invited to participate via facsimile; an office was designated as "recruited" when one of its physicians declared intent to participate. In Phase II, an active link to the Intervention module was e-mailed to physicians recruited in Phase I. Recruited physicians were assigned at the time of logon to either a control or Internet CME intervention arm designed to improve Chlamydia screening rates; physicians within the same office were assigned to the same arm of the study. We designated physicians as "participating" when they first engaged the Internet intervention.The study was conducted between February 1, 2002 and December 31, 2002. The intervention included a series of four modules, feedback of performance data and a quality improvement toolbox. The education modules were based upon adult learning and behavior change theory [ 8 ]. Our driving principles included case-based learning [ 9 , 10 ] making programs interactive by adapting to the program learners' readiness-to-change stage [ 11 ] and performance feedback for behavioral motivation and reinforcement [ 12 ] The control condition was a series of four text-based modules on topics unrelated to Chlamydia. Physicians receive 1 category 1 CME credit per module for their participation. The main outcome measure was Chlamydia screening rates.The subanalysis of this trial focuses on the use of email reminders to engage physicians in the online intervention. Physician recruitment occurred from November of 2001 to January of 2002. Following recruitment, the intervention was initiated in February of 2002 via email broadcast to recruited physicians. During 2002, four separate educational modules were offered. Each module was introduced with a series of email announcements followed by email reminders that contained tailored subject line (i.e. Dear Dr. John Smith) and text message containing the URL that would connect the physician directly to the educational module. The first three modules, emphasized: (1) young sexually active women are at high risk for asymptomatic infection that may lead to future serious health consequences; (2) newer urine-based screening allows diagnosis without a pelvic examination; and (3) infection may be effectively treated with a one-dose antibiotic. The fourth module reviewed previously introduced concepts. A total of 33 announcements and reminders were sent to recruited physicians between February 1, 2002 and December 31, 2002, which represents one reminder overall for each 1.5 weeks of the study duration. Initially, we were concerned that frequent email reminders would be considered intrusive. After a trial period, we found that we could increase the frequency of reminders without difficulty, thus fewer email reminders were sent during the initial phases of the study.For the subanalysis of this trial, the principal outcome measure is participation, defined as physician log-on at least once to the website. Data was collected electronically when physicians logged on to the intervention. In addition, several evaluation questions were used at the conclusion of the online educational activities to explore CME preferences. Descriptive analyses of patient and physician demographics are used to compare baseline characteristics of patients and physicians in the email participants versus the recruited non-participants. Statistical significance is determined with tests appropriate to the distribution of the data (chi-square for categorical variables and student-t test for continuous variable). Two-tailed tests are used for all analyses.Results and discussion Four hundred eighty physicians were recruited to participate, representing 380 physician offices. Of the 463 recruited physicians, 445 were successfully contacted by email using the addresses they had furnished at the time of recruitment. Of these 445 recruited physicians, 210 (47.2%) physicians from 190 offices logged on to at least one of the educational modules. Of the 210 physicians who logged on at least once during the 45-week study period, one hundred twenty-four (59%) returned again to log-on for Module 2, eighty-seven (41%) logged on for Module 3, and forty-four (21%) logged on to Module 4. Two hundred and ten physicians of 445 logged on at least once to the website, leaving 235 physicians as non-participants. Figure  1  represents total physician log-on by week. Analysis of log-on days indicated that participants were most likely to log-on on Monday or Thursday (see Figure  2 ). Log-on times were also examined and findings indicate that physicians were most likely to log-on to a module between the hours of 3 P.M. and 7 P.M (15:00–19:00). Other common times for participants to log-on included times earlier in the day, or between the hours of 8 P.M. and midnight (20:00–24:00) (see Figure  3 ). Figure 1 Cumulative internet engagement by physician over time Figure 2 Number of logins by day of the week. Figure 3 Number of logins by time of day. The participant characteristics (n = 210) were compared with those of recruited but non-participating physicians (n = 235) (Table  1 ). Age was not significant, however there were significant differences by gender, degree, and country of medical training. By race, 81.5% of the participants were Caucasian, 8.8% were Asian, 3.0% were African American, 3.5% were Hispanic and 3.0% were listed as other with no significant differences. The largest percentage of recruited physicians was family practitioners (41.3%), followed by general internists (29.4%), pediatricians (9.6%), and general practitioners (1.5%), with no significant differences. Female physicians were significantly more likely to participate than males (p = . 0001), Medical Doctors (MDs) were significantly more likely than Doctors of Osteopathy (DOs) to participate (p = . 01), and graduates of U.S. medical schools significantly more likely than graduates of international medical schools to participate (p = . 01). In addition to demographic characteristics, chlamydia screening rates of participant and non-participant physicians were compared. Baseline screening rates of nonparticipants were significantly lower than those of participants. Non-participant chlamydia screening rates were 14.6% at baseline, compared to 17.4% for participants (p < .006). Table 1 Participant* versus recruited** but non-participant characteristics Recruited Non-participants Participants p-value N 235 210 Mean Age 44.3 45.2 .143 Gender Male 60.0% 40.0% .0001 Female 40.0% 60.0% Degree DO 65.3% 34.7% .01 MD 51.9% 48.0% Medical Training International 67.5% 32.5% .01 USA 52.7% 47.3% *Participated physician engaged in at least one module **Eligible offices had at least 1 eligible physicians with at least 20 female patients who were candidates for Chlamydia screening according to the Health Employers Data and Information Set Technical Specifications, 2000. From follow-up evaluation question data, 100% of responding DOs felt that the course email reminders were effective in reminding them about educational modules compared to 92.6% of MDs; 95.9% of US medical graduates rated the reminders as useful, while only 77.8% of graduates from non-US medical schools found them useful. Concerning preferences for delivery of CME, no DOs reported web-based activities as their preferred method for lifelong learning; they preferred local (50.0%) and national meetings (50.0%). MDs were more likely to prefer web-based CME (37.0%) to local (35.1%) or national (16.6%) meetings. Female physicians reported a preference for web-based CME (50.0%), whereas male physicians preferred local (35.0%) and national (27.5%) meetings over web-based CME (25.0%). The results of this study indicate that email reminders may be useful in engaging nearly half of a group of practicing primary care physicians recruited to participate in an online women's health educational series. This data is consistent with McMahon et al.'s findings in comparing the use of email, fax and mail, finding that email reminders were more useful to increase response rates [ 12 ]. The study participation rate, (47.2%) is also consistent with the work of Flanagan et. al.'s study of participation in web decision support tools for the management of pneumonia [ 6 ]. However, the gap of up to 3 months between recruitment and the initiation of the online educational activities may have contributed to a lower participation rate. It is possible that by decreasing the gap in time between recruitment and announcement of the availability of the online educational activity, participation rates could be increased. Future study designs using email reminders should consider beginning the intervention immediately following agreement to participate or shortly thereafter. Two current studies using email reminders to promote educational courses in the prevention of glucocorticoid-induced osteoporosis and in the secondary prevention of cardiovascular disease in patients following a myocardial infarction have been designed to deliver the intervention immediately following agreement to participate [ 13 ]. Findings from follow-up evaluation question data indicate that CME providers interested in targeting specific groups of physicians may benefit from using alternative methods of CME recruitment and delivery. CME providers targeting DOs may want to explore ways to engage DOs in web-based learning activities or consider focusing activities that target DOs to local or national meetings. Providers of CME who are interested in engaging male physicians and graduates of U.S. medical schools may find email reminders useful, but they may also want to explore additional methods of recruitment. Persistent email reminders did increase physicians' response rates to online education, but response rate decreased with the number of reminders. The first three reminders produced the largest responses, with decline after the 10 th  reminder. Based on our experience, it would seem reasonable that providers and researchers with limited resources consider focusing their announcements/reminders on the first 3–10 encounters. Data from time of log-on underscores the advantages of asynchronous online interventions for busy clinicians. Traditional "live" online symposia scheduled for the middle of the day might appeal to the physicians who logged on between 10 AM and 2 PM (10:00–14:00), but data from this intervention suggest that many physicians have more available time later in the day for online educational activity. The investigators findings of Monday being a frequent day for log-on was unexpected, but may offer an opportunity for future study designs to include weekend email broadcasting rather than a Thursday broadcast. The topic of the online educational activity may influence response to email announcements and reminders. While baseline Chlamydia screening rates were relatively low in both groups, the significant difference between the groups may indicate that those who are likely to perform better according to clinical practice guidelines are more likely to participate in online educational strategies that reinforce their use. Or the higher screening rates may be associated with a higher degree of interest in the overall topic area of women's health. Also related to the topic addressed in this online study, previous studies of preventive practices of female physicians have indicated they are more likely than males to promote preventive practices [ 14 ] and screening [ 15 ] including Chlamydia screening among their female patients than are male physicians. The advertised educational topic for this study was an online women's health course. More female physicians than male physicians responded to the email course reminders, but the topic may have had more appeal to female physicians than to male physicians, leaving the issue of whether there are gender differences among physicians in response to email reminders unresolved. Comparisons of characteristics of participant physicians and non-participant recruited physicians may be useful to those designing online recruitment and engagement strategies for future studies. Those using email reminders to communicate with physician populations including large numbers of DOs, however, may benefit from considering blended methods of CME recruitment and delivery. Using various methods of reaching providers, may also enhance DO participation. CME providers targeting DOs may want to explore additional ways to engage DOs in web-based learning activities or consider focusing activities that target DOs at local or national meetings.
Results and discussion
Four hundred eighty physicians were recruited to participate, representing 380 physician offices. Of the 463 recruited physicians, 445 were successfully contacted by email using the addresses they had furnished at the time of recruitment. Of these 445 recruited physicians, 210 (47.2%) physicians from 190 offices logged on to at least one of the educational modules. Of the 210 physicians who logged on at least once during the 45-week study period, one hundred twenty-four (59%) returned again to log-on for Module 2, eighty-seven (41%) logged on for Module 3, and forty-four (21%) logged on to Module 4.Two hundred and ten physicians of 445 logged on at least once to the website, leaving 235 physicians as non-participants. Figure  1  represents total physician log-on by week. Analysis of log-on days indicated that participants were most likely to log-on on Monday or Thursday (see Figure  2 ). Log-on times were also examined and findings indicate that physicians were most likely to log-on to a module between the hours of 3 P.M. and 7 P.M (15:00–19:00). Other common times for participants to log-on included times earlier in the day, or between the hours of 8 P.M. and midnight (20:00–24:00) (see Figure  3 ).The participant characteristics (n = 210) were compared with those of recruited but non-participating physicians (n = 235) (Table  1 ). Age was not significant, however there were significant differences by gender, degree, and country of medical training. By race, 81.5% of the participants were Caucasian, 8.8% were Asian, 3.0% were African American, 3.5% were Hispanic and 3.0% were listed as other with no significant differences. The largest percentage of recruited physicians was family practitioners (41.3%), followed by general internists (29.4%), pediatricians (9.6%), and general practitioners (1.5%), with no significant differences. Female physicians were significantly more likely to participate than males (p = . 0001), Medical Doctors (MDs) were significantly more likely than Doctors of Osteopathy (DOs) to participate (p = . 01), and graduates of U.S. medical schools significantly more likely than graduates of international medical schools to participate (p = . 01). In addition to demographic characteristics, chlamydia screening rates of participant and non-participant physicians were compared. Baseline screening rates of nonparticipants were significantly lower than those of participants. Non-participant chlamydia screening rates were 14.6% at baseline, compared to 17.4% for participants (p < .006).Participant* versus recruited** but non-participant characteristics*Participated physician engaged in at least one module**Eligible offices had at least 1 eligible physicians with at least 20 female patients who were candidates for Chlamydia screening according to the Health Employers Data and Information Set Technical Specifications, 2000.From follow-up evaluation question data, 100% of responding DOs felt that the course email reminders were effective in reminding them about educational modules compared to 92.6% of MDs; 95.9% of US medical graduates rated the reminders as useful, while only 77.8% of graduates from non-US medical schools found them useful. Concerning preferences for delivery of CME, no DOs reported web-based activities as their preferred method for lifelong learning; they preferred local (50.0%) and national meetings (50.0%). MDs were more likely to prefer web-based CME (37.0%) to local (35.1%) or national (16.6%) meetings. Female physicians reported a preference for web-based CME (50.0%), whereas male physicians preferred local (35.0%) and national (27.5%) meetings over web-based CME (25.0%).The results of this study indicate that email reminders may be useful in engaging nearly half of a group of practicing primary care physicians recruited to participate in an online women's health educational series. This data is consistent with McMahon et al.'s findings in comparing the use of email, fax and mail, finding that email reminders were more useful to increase response rates [ 12 ]. The study participation rate, (47.2%) is also consistent with the work of Flanagan et. al.'s study of participation in web decision support tools for the management of pneumonia [ 6 ]. However, the gap of up to 3 months between recruitment and the initiation of the online educational activities may have contributed to a lower participation rate. It is possible that by decreasing the gap in time between recruitment and announcement of the availability of the online educational activity, participation rates could be increased. Future study designs using email reminders should consider beginning the intervention immediately following agreement to participate or shortly thereafter. Two current studies using email reminders to promote educational courses in the prevention of glucocorticoid-induced osteoporosis and in the secondary prevention of cardiovascular disease in patients following a myocardial infarction have been designed to deliver the intervention immediately following agreement to participate [ 13 ].Findings from follow-up evaluation question data indicate that CME providers interested in targeting specific groups of physicians may benefit from using alternative methods of CME recruitment and delivery. CME providers targeting DOs may want to explore ways to engage DOs in web-based learning activities or consider focusing activities that target DOs to local or national meetings. Providers of CME who are interested in engaging male physicians and graduates of U.S. medical schools may find email reminders useful, but they may also want to explore additional methods of recruitment.Persistent email reminders did increase physicians' response rates to online education, but response rate decreased with the number of reminders. The first three reminders produced the largest responses, with decline after the 10 th  reminder. Based on our experience, it would seem reasonable that providers and researchers with limited resources consider focusing their announcements/reminders on the first 3–10 encounters. Data from time of log-on underscores the advantages of asynchronous online interventions for busy clinicians. Traditional "live" online symposia scheduled for the middle of the day might appeal to the physicians who logged on between 10 AM and 2 PM (10:00–14:00), but data from this intervention suggest that many physicians have more available time later in the day for online educational activity. The investigators findings of Monday being a frequent day for log-on was unexpected, but may offer an opportunity for future study designs to include weekend email broadcasting rather than a Thursday broadcast.The topic of the online educational activity may influence response to email announcements and reminders. While baseline Chlamydia screening rates were relatively low in both groups, the significant difference between the groups may indicate that those who are likely to perform better according to clinical practice guidelines are more likely to participate in online educational strategies that reinforce their use. Or the higher screening rates may be associated with a higher degree of interest in the overall topic area of women's health.Also related to the topic addressed in this online study, previous studies of preventive practices of female physicians have indicated they are more likely than males to promote preventive practices [ 14 ] and screening [ 15 ] including Chlamydia screening among their female patients than are male physicians. The advertised educational topic for this study was an online women's health course. More female physicians than male physicians responded to the email course reminders, but the topic may have had more appeal to female physicians than to male physicians, leaving the issue of whether there are gender differences among physicians in response to email reminders unresolved.Comparisons of characteristics of participant physicians and non-participant recruited physicians may be useful to those designing online recruitment and engagement strategies for future studies. Those using email reminders to communicate with physician populations including large numbers of DOs, however, may benefit from considering blended methods of CME recruitment and delivery. Using various methods of reaching providers, may also enhance DO participation. CME providers targeting DOs may want to explore additional ways to engage DOs in web-based learning activities or consider focusing activities that target DOs at local or national meetings.Conclusions Physicians' online clinical information seeking and engagement in online education continues to grow [ 12 ]. Researchers of online interventions who are attempting to improve the quality of healthcare and physician performance should continue to study and evaluate physician online behavior. Knowing when, where, and how physicians seek information on the Internet, and how they respond to receiving specific information pushed toward them, will prove to be very useful for targeting future quality improvement interventions. Reminding physicians often via email about online educational opportunities appears to increase engagement in a community-based primary care physician audience. The early and consistent implementation of this push technology may increase physicians' utilization of interventions designed to improve practice.
Conclusions
Physicians' online clinical information seeking and engagement in online education continues to grow [ 12 ]. Researchers of online interventions who are attempting to improve the quality of healthcare and physician performance should continue to study and evaluate physician online behavior. Knowing when, where, and how physicians seek information on the Internet, and how they respond to receiving specific information pushed toward them, will prove to be very useful for targeting future quality improvement interventions.Reminding physicians often via email about online educational opportunities appears to increase engagement in a community-based primary care physician audience. The early and consistent implementation of this push technology may increase physicians' utilization of interventions designed to improve practice.Authors' contributions MA participated in the statistical analysis and drafted the manuscript. BCC participated in the statistical analysis and drafting of the manuscript. LC participated in all phases of the project. TW participated in the draft of the manuscript. CS participated in the design and coordination of the study and the drafting of the manuscript. MNR participated in the coordination of the study. NWW participated in the design and implementation of the study. JJA conceived of the study and participated in all phases of the study. All authors read and approved the final manuscript.
Authors' contributions
MA participated in the statistical analysis and drafted the manuscript. BCC participated in the statistical analysis and drafting of the manuscript. LC participated in all phases of the project. TW participated in the draft of the manuscript. CS participated in the design and coordination of the study and the drafting of the manuscript. MNR participated in the coordination of the study. NWW participated in the design and implementation of the study. JJA conceived of the study and participated in all phases of the study. All authors read and approved the final manuscript.Competing interests The authors declare that they have no competing interests.
Competing interests
The authors declare that they have no competing interests.Pre-publication history The pre-publication history for this paper can be accessed here:
Pre-publication history
The pre-publication history for this paper can be accessed here: