Although there are currently 65.4 million pigs in the United States, representing a $22.5 billion industry accounting for 35,000 direct and 515,000 indirect jobs, only a limited pool of veterinarians trained in collecting diagnostic samples from swine would be available in the event of a transboundary, emerging, or zoonotic disease outbreak requiring an emergency response.1,2 For example, when the AVMA surveyed graduates of the class of 2013, only 13% of respondents, or approximately 240 students, reported that they would be entering food animal or mixed animal practice after graduation (the specific number entering swine practice was not reported).3 Average US membership of the American Association of Swine Veterinarians, the only professional organization specifically devoted to swine veterinarians, was approximately 850 from 2012 through 2015, and student membership, which included students in all years of veterinary training, decreased from 407 in 2012 to 344 in 2015.2
The current capacity for response to a public health threat or foreign animal disease outbreak among swine can be estimated by assuming the available pool of veterinarians with training in clinical swine medicine is close to the membership of the American Association of Swine Veterinarians (854 during 2014). The USDA estimated the total hog and pig inventory during 2012 to be 66,026,785 on approximately 63,246 farms.1 Thus, the pigs-to-swine veterinarian ratio is approximately 77,315, and the farms-to-swine veterinarian ratio is approximately 75. With each veterinarian responsible for approximately 75 farms, it would be impossible to perform necessary surveillance or regulatory tasks during an emergency response while also maintaining ongoing herd health and animal welfare programs.
During the spring and summer of 2015, an outbreak of highly pathogenic avian influenza devastated the US poultry industry.4 At the peak of the response to that outbreak, there were approximately 3,440 state, federal, and contracted personnel deployed to the field. Approximately 50 veterinarians or animal health technicians served as temporary employees of the USDA's National Animal Health Emergency Response Corps, and many more volunteered for short terms of duty with their state animal health agencies.4 In addition, the USDA sought to hire an additional 90 veterinarians and 210 animal health technicians for 1- to 2-year assignments during 2015 and 2016.5 The number of veterinarians recruited from outside the poultry industry is unknown, but given that there are fewer than 1,000 veterinarians and veterinary students focused on poultry medicine in the United States,6 it was likely substantial.
Mixed animal veterinarians and, perhaps, companion animal veterinarians and nonveterinarians such as animal health technicians could potentially be recruited to assist in the event of a major swine disease outbreak in the United States. However, these individuals would likely require training in swine-specific sample collection techniques. Of course, such training would need to be highly efficient because time that experts spent training responders would represent time taken away from responding to the outbreak.
The pyramid training method has been shown to be an efficient method for training relatively large numbers of individuals. With this method, an expert trains a small group of individuals who then serve as trainers for a second, larger group. The purpose of the study reported here was to develop and evaluate a pyramid training method for teaching techniques for collection of diagnostic samples from swine.
Materials and Methods
The study protocol was reviewed and approved by both the Institutional Review Board and the Institutional Animal Care and Use Committee at Iowa State University.
With the rationale that, in regard to swine diagnostic sample collection techniques at least, veterinary students would have basic science knowledge and general skills representative of veterinarians who were not involved in swine practice, the decision was made to test the pyramid training method on current veterinary students at the Iowa State University College of Veterinary Medicine. Students in all 4 years of the veterinary curriculum were invited to participate. Individuals who expressed interest in participating were asked to indicate their year in veterinary school and their level of experience with veterinary medical practice in general and swine medicine in particular. Students enrolled in the study were assigned a random number generated from an internet-based random sequence program.a Swine veterinary experts from Iowa State University were trained as evaluators prior to the study.
The study consisted of 3 phases: a preinstruction assessment phase, a daylong instruction phase, and a postinstruction assessment phase.
Preinstruction assessment phase
Prior to the preinstruction assessment, student participants were required to view online videos on animal restraint, use of personal protective equipment, biosecurity, and the 4-circle approach to farm evaluation. All participants then went through a preinstruction assessment to determine their level of familiarity with the equipment needed and techniques used to collect samples of blood, nasal secretions, feces, and oral fluid from pigs. No instruction on the specific sample collection techniques was provided during this phase; however, participants were supervised by a veterinary instructor or trained veterinary student safety officer to ensure student and animal safety and humane handling at all times.
For the preinstruction assessment, participants were provided the supplies necessary to collect samples of blood, nasal secretions, feces, and oral fluid, along with distractor supplies chosen to be similar to the equipment that would normally be used but with features that made the distractor supplies inappropriate for the specific clinical task (Appendix 1).
Each participant was asked to choose the appropriate supplies to collect a sample of blood, nasal secretions, and feces. If appropriate supplies were chosen, the veterinary evaluator allowed the participant to proceed, and an animal was restrained by study staff to allow the participant to collect a sample. At the first deviation from an acceptable sample collection practice, or if safety of the animal or participant was compromised, the procedure was stopped by the evaluator (Appendix 2). For example, if a participant could not select the appropriate blood collection equipment, he or she was asked to stop immediately. If the participant selected the appropriate blood collection equipment, but failed to approach the pig near the desired landmark (eg, approached with the intent to draw blood from the saphenous vein instead of the jugular vein), the procedure was stopped. Even if a participant selected the appropriate equipment, targeted the correct anatomy, and passed all other assessment prerequisites to begin collecting a blood sample, a time limit was imposed to protect animals in the study from the negative effects of prolonged restraint. Participants were given a maximum of 1 minute to collect a nasal swab sample and a maximum of 1 minute to collect a blood sample. As a consequence, a participant could identify the correct equipment and procedure but still fail to collect a useful sample.
After individual evaluations were completed, participants were assigned to groups of 3 and asked to choose the appropriate supplies for collection of an oral fluid sample. Again, at the first deviation from an acceptable sample collection practice, or if safety of the animals or participants was compromised, the procedure was stopped.
After the clinical evaluations were completed, participants took a written quiz consisting of still photographs and a total of 16 written questions that was designed to assess their ability to identify the correct equipment, positioning, and procedures for collection of samples of blood, nasal secretions, feces, and oral fluid.
During the preinstruction phase, participants were asked to not discuss techniques for sample collection with each other, and evaluators were instructed to provide no corrections to participants during the clinical evaluation. Participants were distanced from each other so they were not able to view each other's technique.
Instruction phase
After all preinstruction assessments were completed, the instruction phase, which consisted of both classroom-based and hands-on instruction, commenced. The classroom-based instruction was provided with a portable projector, laptop computer, and projection screen. Participants were shown a series of videos directed by a veterinary expert from the Swine Medicine Education Center that illustrated the correct equipment and techniques for collecting samples of blood, nasal secretions, feces, and oral fluid.
After the classroom-based instruction was completed, participants received hands-on pyramid-based instruction on collection of samples of blood, nasal secretions, and feces. Hands-on instruction was initiated by a single swine veterinarian who trained 2 participants on each of the techniques. Each of these 2 participants trained 2 additional participants, and pyramid training continued in this manner until all participants were trained.
Concurrently, a pyramid training approach was used to demonstrate the proper technique for collection of an oral fluid sample. A single swine veterinarian trained 3 participants to collect oral fluid. Each of these 3 participants trained 3 additional participants, and pyramid training continued in this manner until all participants were trained to collect samples of oral fluid.
At each pyramid level, the instructor demonstrated the proper technique and each trainee practiced sample collection. Trainees were allowed to ask questions of their designated instructor, but were not allowed to ask questions of the original veterinary instructor or the veterinary evaluators and could not consult with an individual in a previous level in the pyramid.
Postinstruction assessment phase
A postinstruction assessment was performed immediately after the instruction phase was completed. Participants were provided the same necessary and distractor supplies provided during the preinstruction assessment and asked to collect samples of blood, nasal secretions, feces, and oral fluid. Clinical evaluations were conducted by the same evaluators, and the same limitations to protect animals and students were applied. Two days later, participants completed, online, the same written quiz they had completed during the preassessment phase.
All animals used in the study were monitored until marketed by veterinary and farm staff for adverse effects associated with the restraint and sample collection procedures.
Results
Participant demographics
Forty-five students enrolled at the Iowa State University College of Veterinary Medicine participated in the study, which was held 1 week after the beginning of the 2015 fall semester. Most (23 [51%]) participants were first-year veterinary students; no fourth-year veterinary students participated. Eight of the 45 (18%) participants reported previous extensive clinical veterinary experience, and 12 (27%) reported little or no previous veterinary experience. Only 1 (2%) participant reported previous extensive swine experience, and 22 (49%) reported no previous swine experience. Participants reported a range of academic interests, including small animal practice (n = 6), equine practice (1), food animal practice (13), mixed animal practice (16), other practice (1), laboratory animal or exotic animal practice (5), public health (1), and research (2).
Preinstruction assessment
During the preinstruction assessment phase, only 2 (4%) participants demonstrated the proper blood sample collection technique. Few could collect adequate fecal (12 [27%]) or nasal secretion (9 [20%]) samples, and only 2 of the 15 groups (3 participants/group) successfully collected an oral fluid sample. None of the participants recognized all 4 correct sample collection techniques from photographs and written assessments, and only 23 (51%) identified the correct location for venipuncture in a pig (ie, right vena cava) when presented with a series of photographs. Four (9%) participants did not recognize a rope (vs a swab, dust cloth, or speculum) as the most appropriate equipment for collecting oral fluid samples. However, most (37 [84%]) recognized the most appropriate method for transporting nasal and fecal samples. Written quiz scores ranged from 35% to 76% with a mean of 57%.
Postinstruction assessment
During the postinstruction assessment phase, 27 (60%) participants demonstrated the proper technique for blood sample collection and were able to collect a useful clinical sample. All 45 participants selected the appropriate supplies for blood sample collection and indicated the correct needle placement. In addition, all 45 participants were able to successfully collect fecal and nasal samples. After instruction, all 15 groups (3 participants/group) were able to successfully collect oral fluid samples. Written quiz scores ranged from 44% to 100% with a mean of 79%.
No evidence that animals were adversely affected by the restraint or sampling collection procedures was observed. All animals continued to their intended use or marketing end point, as determined prior to the study.
Discussion
Following the instruction phase, veterinary students who participated in the study showed a substantial increase in technical skill, as evidenced by the increase in percentages of participants able to collect adequate samples of blood, nasal secretions, feces, and oral fluid. The participants' clinical knowledge also improved, as evidenced by the increase in scores on a written quiz assessing their ability to identify the correct equipment, positioning, and procedures for collection of those samples. These findings suggested that in the event of a transboundary, emerging, or zoonotic disease outbreak, this training method could potentially alleviate the strain on swine veterinarians by quickly and efficiently increasing the number of individuals available to collect necessary diagnostic samples.
It was not unexpected that participants in the present study performed poorly prior to instruction, given that they were veterinary students who generally had little clinical experience. Although participants might not have known the correct technique during the preinstruction assessment phase, their creativity was apparent. For example, 1 student planned to collect a fecal sample from a pig by inserting a plastic spoon into the rectum (to protect the pig, the student was stopped before attempting the procedure). To collect oral fluids, multiple groups of participants hung a rope, then swabbed the rope with a swab or dust cloth. Other groups tried to restrain pigs with hog snares or with the ropes intended for collection of oral fluid samples.
The clinical and written evaluations performed during the pre- and postinstruction assessment phases sought to assess 2 necessary components of successful diagnostic sample collection: technical skill and clinical knowledge. The clinical evaluation assessed whether students had the technical skills necessary to collect adequate samples. The written evaluation assessed whether students had the appropriate knowledge base required to competently perform the collection techniques. The improvement in written test scores 2 days after the instruction period suggested that knowledge both increased and was retained. Thus, although more practice might have been needed to consistently collect samples, participants had an improved understanding of the techniques. Note that the true technical improvement was likely underestimated in the present study because time restrictions were placed on collection of blood samples and nasal secretions.
The USDA recognizes private veterinary practitioners as having a role in federal and international veterinary medicine through the National Veterinary Accreditation Program, with accredited veterinarians performing regulatory duties and helping control disease.7 In addition to meeting the 16 core competencies established by the USDA, accredited veterinarians must also be proficient in new sampling techniques, unusual testing or screening methods, or new methods of test interpretation required by certain diseases. The pyramid training method described in the present report may be useful in helping veterinarians meet these additional requirements, as it seems likely the method could be adapted to any species, any disease, and any clinical technique.
Federal, state, and local health agencies have been urged to provide more opportunities to prepare rural veterinarians for bioterrorism response,8 and hands-on training incorporating a pyramid training method could potentially be a way to accomplish this. The pyramid training method used in the present study was developed with the intent that it could be deployed with limited resources and personnel. The primary mode of instruction involved prerecorded videos developed at Iowa State University, with only a single veterinary instructor initiating pyramid training.
Importantly, although the pyramid training method in the present study resulted in an overall improvement in technical skills and clinical knowledge, the quality of instruction at the top of the pyramid was not compared with the quality at the bottom. An expanded study would be required to evaluate this.
In summary, our findings suggested that in the event of a transboundary, emerging, or zoonotic disease outbreak, the pyramid training method could help alleviate the strain on swine veterinarians and conserve resources while quickly and efficiently increasing diagnostic sampling capacity. Although tested with swine, the same training method could be applied during disease outbreaks affecting any food animal species.
Acknowledgments
Supported by the Douglas and Ann Gustafson Professorship for Excellence in Veterinary Education at Iowa State University. No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
Presented in part at the 47th Annual Meeting of the American Association of Swine Veterinarians, New Orleans, February 2016.
Footnotes
Random sequence generator, Randomness and Integrity Services Ltd, Dublin, Ireland. Available at: www.random.org/sequences/. Accessed Aug 28, 2015.
References
1 USDA. 2012 census of agriculture, May 2014 edition. Available at: www.agcensus.usda.gov. Accessed Sep 1, 2015.
2 American Association of Swine Veterinarians. AASV board meeting minutes. Available at: www.aasv.org/aasv/board. htm. Accessed Apr 26, 2016.
3 Shepherd AJ, Pikel L. Employment, starting salaries, and educational indebtedness of year-2013 graduates of US veterinary medical colleges. J Am Vet Med Assoc 2013; 243: 983–987.
4 Cima G. Devastating flu, ongoing harm. J Am Vet Med Assoc 2015; 247: 434–439.
5 USDA hiring veterinarians to fight avian flu. J Am Vet Med Assoc 2015; 247: 439.
6 American Association of Avian Pathologists. Available at: www.aaap.info. Accessed Jan 25, 2016.
7 Wenzel JGW, Wright JC. Veterinary accreditation and some new imperatives for national preparedness. J Am Vet Med Assoc 2007; 230: 1309–1312.
8 Hsu CE, Jacobson H, Feldman K, et al. Assessing bioterrorism preparedness and response of rural veterinarians: experiences and training needs. J Vet Med Educ 2008; 35: 262–268.
Appendix 1
Necessary and distractor supplies used to test veterinary students' knowledge of clinical techniques for collection of diagnostic samples from swine.
| Sample | Necessary supplies | Distractor supplies |
|---|---|---|
| Nasal secretions | Sterile, nylon-flocked swab Snap-cap test tube (PBS solution) | Dust cloth 15-mL conical centrifuge tube Snap-cap test tube (empty) |
| Feces | Plastic spoon 50-mL conical centrifuge tube | Disposable plastic sleeve Test tube (EDTA) Sterile sample bag |
| Blood | 12-mL syringe Serum separator tube 16-gauge, 1.5-in sterile needle | 3-mL syringe 20-gauge, 0.75-in sterile needle |
| Oral fluid | Cotton rope 50-mL conical centrifuge tube Plastic zip-top bag | Sterile, nylon-flocked swab Dust cloth |
Appendix 2
Criteria used to assess technical skills of veterinary students during collection of diagnostic samples from swine.
| Sample | Nonacceptable technique | Inadequate technique | Acceptable technique |
|---|---|---|---|
| Nasal secretions Supply selection | Incorrect supplies (anything but swab) selected* | NA | Swab selected |
|   Quality of technique | Too shallow or too deep insertion of swab or touched skin†| Adequate technique but only 1 nostril swabbbed | Both nostrils swabbed to an adequate depth while avoiding touching skin |
|   Time taken | > 1 min* | 30 s to 1 min | < 30 s |
|   Transport selection | Snap-cap tube without PBS solution or centrifuge tube | NA | Snap-cap test tube containing PBS solution |
| Blood | |||
|   Supply selection | Inappropriate needle (20-gauge, 0.75-in needle)* | Appropriate needle (16-gauge, 1.5-in needle) but inappropriate syringe (3 mL) | Appropriate needle (16-gauge, 1.5-in needle) and syringe (12 mL) |
|   Needle placement | Incorrect placement* | NA | Proper placement in right jugular furrow |
|   Time taken | > 1 min* | 30 s to 1 min | < 30 s |
|   Sample quantity | < 1 mL | 1 to 4 mL | ≥ 5 mL |
| Feces | |||
|   Sample location and quality | Sample collected from alley with hands or scooped with conical tube | NA | Sample collected directly from pig or from fresh manure piles in pen |
|   Sample quantity | < 5 mL or < 10 g | NA | ≥ 5 mL or ≥ 10 g |
|   Storage container | Sterile sample bag, test tube, or disposable sleeve | NA | Conical centrifuge tube |
| Oral fluid | |||
|   Placement of rope | Rope hung too high or too low | Rope hung near feeders | Rope hung at appropriate height (pigs' shoulder height) and away from feeders |
|   Storage technique | Handled rope before or after collection without gloves, left rope in bag, or transferred rope directly to conical tube | NA | Did not handle rope without gloves and transferred rope to conical tube for transport |
Participant was not allowed to proceed with nasal or blood sample collection.
Appropriate depth for nasal swab insertion was approximately 3 to 4 cm.
NA = Not applicable.
