We believe that we have resolve the issue at this time. I will outline the cause/resolution below in case anyone else has the same problem.
Cause:
On all of our virtual servers, and pool members we are using cookie persistance. While trying to diagnose the problem, we started to look into "oneconnect" profiles, and found a note in the article here http://support.f5.com/kb/en-us/solu...l7208.html
Resolution:
We created a new oneconnect profile, and assigned in to the virtual servers that were effected by this. We used the following link as our reference http://support.f5.com/kb/en-us/solu...l7964.html
After applying a oneconnect profile to our virtual servers, the random 400 errors seem to no longer occur. If I understand the article correctly, this would only occur if you are using "cookie" or "universal" persistance methods.