Abstract
The thoracic pump and the abdominal pump are osteopathic manipulative (OM) lymphatic pump techniques frequently used by osteopathic physicians to treat patients with infections (eg, pneumonia, otitis media). Although there is a widely accepted belief among the osteopathic medical profession that increasing lymphatic flow is beneficial, no measurements of lymph flow during osteopathic manipulative treatment have been reported. The authors surgically instrumented five mongrel dogs to record lymphatic flow in the thoracic duct (TDF) and cardiac variables during three intervention protocols. After recovery from surgery, canine subjects were placed in a standing-support sling, and TDF, cardiac output, mean aortic blood pressure, and heart rate were recorded during two randomized 30-second sessions of manipulative intervention using the osteopathic thoracic pump and abdominal pump techniques on two successive days. Lymph flow in the thoracic duct increased from 1.57±0.20 mL·min-1 to a peak TDF of 4.80±1.73 mL·min-1 during abdominal pump, and from 1.20±0.41 mL·min-1 to 3.45±1.61 mL·min-1 during thoracic pump. Lymph flow in the thoracic duct and cardiac variables were also recorded for canine subjects during physical activity (ie, treadmill exercise at 3 miles per hour at 0% incline). During physical activity, TDF increased from 1.47±0.33 mL·min-1 to 5.81±1.30 mL·min-1. Although cardiac variables did not change significantly during manipulative intervention with lymphatic pump techniques, cardiac output and heart rate did increase during physical activity. The authors conclude that physical activity and manipulative intervention using thoracic pump and abdominal pump techniques produced net increases in TDF (P<.05).
Manual techniques with a goal of increasing lymphatic flow have long been a focus in the practice of osteopathic medicine.
1,2 Andrew Taylor Still, MD, DO, recognized the importance of the lymphatic system and dedicated an entire chapter to this topic in
Philosophy of Osteopathy (1899), writing, “Thus we strike at the source of life and death when we go to the lymphatics.”
3
Lymphatic treatments continue to be an important component of osteopathic manipulative medicine. Miller
4 developed the lymphatic pump in 1926, stating that it is “an exaggeration of the movements of respiration.” The lymphatic pump technique is used to treat patients with edema and infections because increasing lymphatic flow improves the filtering and removal of fluid, inflammatory mediators, and waste products from interstitial space.
During the influenza pandemic of 1917, Smith
5 reported that osteopathic manipulative treatment (OMT) decreased the mortality rate from 5% to 0.25% among 100,000 patients.
Although it has been widely accepted by the osteopathic medical profession that increasing lymphatic flow is beneficial,
6 no direct measurements of lymph flow during OMT have been reported—though there have been reports of beneficial clinical responses to lymphatic pump treatments that may have resulted from increased lymph flow.
6–15
In 1920, for example, Lane
7 found that performing the splenic pump—another lymphatic pump technique—on two rabbits injected with washed sheep blood corpuscles increased antibody content in the serum. Sleszynski and Kelso
8 demonstrated more recently that, in patients recovering from cholecystectomy, the lymphatic pump more rapidly returns forced vital capacity and forced expiratory volume in one second toward preoperative values as compared with incentive spirometry. Mesina et al
9 showed that lymphatic pump techniques, including pectoral traction and splenic pump, elicit transient basophilia of varying degree and duration in healthy men. In elderly patients hospitalized with pneumonia, Noll et al
10 used a standardized OMT protocol that included the application of the thoracic pump technique. Using these techniques, Noll et al
10 reduced the duration of patients' use of oral antibiotics in addition to demonstrating a tendency to reduce mean duration of leukocytosis, intravenous antibiotic treatment, and the length of patients' hospital stays. By showing an increase in antibody response to pneumococcal polysaccharide following OMT, Measel
11 reported that healthy patients receiving OMT with thoracic pump treatments demonstrated a statistically significant improvement in immune response over those not receiving this treatment modality. In addition, subjects receiving lymphatic and splenic pump treatments during hepatitis B vaccination demonstrated consistently higher antibody titers compared with those not receiving OMT, according to a study by Jackson et al.
12 In a detailed review of the literature concerning the effects of OMT on the lymphatic system, Dengenhardt and Kuchera
6 note the need for additional studies designed to test the direct effects of OMT on lymphatic circulation.
Dery et al
13 injected albumin labeled with a fluorescent probe into the hind limbs of laboratory rats. The presence of the fluorescent probe in blood samples from the rats' tails was used as an index of lymphatic flow. When researchers applied intermittent manual pressure to the thorax of laboratory rats, however, they found that the concentration of the fluorescent probe increased in the blood samples they were taking, indicating an increase in the probe's transport through the lymphatic system.
13
Lymphatic flow has also been measured after cannulation of the thoracic duct,
14 but this direct thoracic technique has not been used to investigate responses to manual medicine in animal or human studies. Cannulation and collection of lymph as a means of assessing lymph flow has been criticized by Onizuka et al,
15 who suggest that cannulation may alter the normal pumping action of the thin-walled thoracic duct.
In the present study, an ultrasonic flow transducer was surgically implanted and used to measure lymph flow in the thoracic duct (TDF) in conscious canine subjects at rest and during manipulative intervention and physical activity. A similar approach was used by Onizuka et al
15 to study lymph flow patterns in sheep. Increased TDF has been previously demonstrated in canine subjects during physical activity.
16,17 Therefore, in our study design, we chose to have dogs undergo physical activity in the form of mild treadmill exercise to measure changes in TDF and to compare them with any changes in TDF levels produced by manipulative intervention.
The aim of the present study was to measure the effect of two types of manipulative intervention on TDF in conscious, surgically instrumented canine subjects, testing a longstanding premise of osteopathic principles and practice.
The day before surgery, a weight-dependent dose of cephalexin, 35 mg per kg, was administered subcutaneously to canine subjects to help prevent postsurgical infection. On the day of surgery, acepromazine maleate (0.03 mg/kg) was provided subcutaneously as a preanesthetic. Thirty minutes later, an intravenous line was placed in subjects' antecubital vein, and thiopental sodium, 5 mg per kg, was administered. After endotracheal intubation, a surgical plane of anesthesia was maintained in canine subjects by mechanical ventilation with supplemental oxygen and isoflurane (1% to 3%). A left lateral thoracotomy was performed on canine subjects in the fifth intercostal space. A 17-gauge catheter was then implanted through a purse-string suture into the descending aorta to measure mean aortic blood pressure (BP). A 1-cm to 2-cm section of the thoracic duct was isolated at the level of the heart for placement of a 2.0-mm or 2.5-mm diameter perivascular flow transducer (model 2SB/2.5SB; Transonic Systems Inc, Ithaca, NY). Another flow transducer was placed around the ascending aorta to measure cardiac output. The catheter and the flow transducers were secured by suture to surrounding tissue.
At the conclusion of instrumentation, the catheter and the flow transducer cables were tunneled subcutaneously and exteriorized between the scapulae. A chest tube was inserted to evacuate the pneumothorax after chest closure. To minimize postoperative pain, 2.5% bupivacaine was sprayed at the point of incision immediately before closure, and buprenorphine hydrochloride (0.03 mg/kg) was administered intramuscularly. After the final layer of skin was closed with staples, triple antibiotic ointment (neomycin sulfate, polymyxin B sulfate, and bacitracin zinc) was applied to the surgical wound. Finally, the dogs' chests were wrapped with veterinary wrap bandages, and nylon jackets were used to protect the catheter and flow transducer cables.
After recovery from surgery, canine subjects were placed in a standing-support sling, and TDF levels, cardiac output, and BP and were recorded. Mean aortic blood pressure was measured by connecting a pressure transducer (model 1290C; Hewlett-Packard Development Company LP, Palo Alto, Calif) to the aortic catheter at the level of the heart. Output from the aortic pressure transducer and the flow transducers on the thoracic duct and the aorta were recorded on a multichannel chart recorder (model 7758; Hewlett-Packard Development Company LP, Palo Alto, Calif) and on a data acquisition system (version 1.8.5; EMKA Technologies, Falls Church, Va), which computed heart rate from the aortic pressure pulse. All baseline TDF data and cardiac variables were collected with the canine subjects in the standing-support sling.
Previous animal studies have examined the effects of manipulative intervention on lymphatic flow only indirectly.
13 In the present study, implantation of a perivascular flow transducer on the thoracic duct enabled us to gather accurate measurements of TDF levels so that the immediate effects of manipulative intervention could be studied. Both manipulative interventions used in our study protocol produced significant increases in TDF levels (
P<.05).
Values for TDF have been reported for more than 100 years in experiments using cannulation of the thoracic duct. In a 1997 investigation, Onizuka et al
15 note TDF rates of 2 mL·kg
–1·hour
-1 in anesthetized dogs and 3 mL·kg
–1·hour
-1 in anesthetized sheep documented in two early studies, performed in 1871 and 1873, respectively.
15 The baseline flow levels from the present study are slightly higher, at 4 mL·kg
–1·hour
-1. Onizuka et al
15 measured baseline lymphatic flows of 5.4±3.1 mL·min
-1 in unanesthetized adult sheep using a Transonics flow transducer implanted on the thoracic duct, an instrumentation technique similar to the one we used for the present study. Onizuka et al
15 reported TDF values that were slightly higher than those observed in the present study of canines. These higher TDF values may be explained by the larger relative size of sheep or other species-related differences.
In addition to measuring TDF levels during the manipulative intervention techniques previously described, we also attempted to measure TDFs while using the pedal pump technique. This technique, however, required laying canine subjects on their backs in the standing-support sling. It was very difficult to keep the dogs relaxed in this position. In addition, we found it was necessary to modify the pedal pump technique for canine subjects because they are not able to lock their hind legs in an extension position as are human subjects. Because of this necessary modification to established OM techniques, the procedure as applied to canine subjects no longer accurately corresponded with the technique as performed on patients in the clinical setting. Although the modified pedal pump technique remained capable of producing increases in TDF levels for canine subjects, we chose not to report those data in the context of the present study because we feel that the required modifications in technique make those results not applicable to human patients.
In the two canine subjects for which recovery data was gathered (ie, canine subjects 4 and 5), TDF levels quickly returned to baseline levels following the termination of manipulative intervention. Although this observation demonstrates the ability of researchers to measure changes in TDFs accurately, it also suggests that these OM techniques, when used in the clinical setting for OMT, may not have sustained effects after treatment is completed. However, the fact that TDF levels were increased throughout manipulative intervention suggests that more frequent and/or more prolonged use of these OM techniques may have more substantial clinical benefits.
Individual approaches to patient management with the use of lymphatic pump treatments vary from patient to patient and physician to physician. In hospitalized patients, treatments may be performed daily, but they may only be done weekly in the outpatient setting. Because patients with edema and infection have impaired lymphatic function, applying lymphatic pump techniques more frequently may more effectively reduce lymph stasis (or lymph congestion) and restore adequate lymphatic function.
Further, by increasing the duration of intervention with the abdominal pump technique in one canine subject (canine subject 1) from 30 seconds to 240 seconds, TDF levels were maintained at increased rates during this prolonged manipulative intervention. This beneficial outcome suggests the need for additional studies to examine the optimal duration of OMT using thoracic and abdominal pump techniques to increase TDFs. In addition, further studies should be performed to gather information concerning the most effective rates of compression and the optimal combination of lymphatic pump treatments.
Although TDF levels increased significantly with manipulative intervention in this canine study, the clinical ramifications of this increase cannot be adequately evaluated from the present data. More studies must be completed to demonstrate that increases in TDFs produced by lymphatic pump techniques can significantly reduce peripheral edema or improve recovery from infection. The composition and source of the lymph that is mobilized upon application of lymphatic pump techniques would also be an important focal point for future investigations. Because lymphatic pump techniques are known to improve the immune response to pneumococcal polysaccharide
11 and hepatitis B vaccination
12 in humans, it is possible that the lymphatic pump techniques may have beneficial and preventive effects beyond that of increasing lymphatic transport.
This preliminary canine study is the first to show direct, realtime increases in TDF during manipulative intervention. It is our hope that the present findings will stimulate additional osteopathic medical research in this area. Replication of these results with subsequent linking to positive clinical benefits would further support the use of lymphatic pump techniques as additional low-cost, low-technology means of treating infection in humans.
Funding for this project was provided by the Osteopathic Research Center in Fort Worth, Tex, and the National Institutes of Health's National Center for Complementary and Alternative Medicine (Grant No. P01 AT 2023) in Bethesda, Md. The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of the National Center for Complementary and Alternative Medicine.
Amalfitano DM. The osteopathic thoracic-lymphatic pump: a review of the historical literature. J Osteopath Med. April–May 1987;1:20-24.
Chikly BJ. Manual techniques addressing the lymphatic system: origins and development. J Am Osteopath Assoc. 2005;105:457-464.
Miller CE. The lymphatic pump, its application to acute infections. J Am Osteopath Assoc. 1926;25(Pt 1):443-445.
Smith RK. One hundred thousand cases of influenza with a death rate of one-fortieth of that officially reported under conventional medical treatment. J Am Osteopath Assoc. 1920;19:172-175.
Degenhardt BF, Kuchera ML. Update on osteopathic medical concepts and the lymphatic system [review]. J Am Osteopath Assoc. 1996;96:97-100.
Lane MA. On increasing the antibody content of the serum by manipulation of the spleen. J Osteopath. 1920;27:361-364.
Sleszynski SL, Kelso AF. Comparison of thoracic manipulation with incentive spirometry in preventing postoperative atelectasis. J Am Osteopath Assoc. 1993;93:834-838, 843-845.
Mesina J, Hampton D, Evans R, Ziegler T, Mikeska C, Thomas K, et al. Transient basophilia following the application of lymphatic pump techniques: a pilot study. J Am Osteopath Assoc. 1998;98:91-94.
Noll DR, Shores J, Bryman PN, Masterson EV. Adjunctive osteopathic manipulative treatment in the elderly hospitalized with pneumonia: a pilot study. J Am Osteopath Assoc. 1999;99: 143-146, 151-152.
Measel JW Jr. The effect of the lymphatic pump on the immune response: I. Preliminary studies on the antibody response to pneumococcal polysaccharide assayed by bacterial agglutination and passive hemagglutination. J Am Osteopath Assoc. 1982;82:28-31.
Jackson KM, Steele TF, Dugan EP, Kukulka G, Blue W, Roberts A. Effect of lymphatic and splenic pump techniques on the antibody response to hepatitis B vaccine: a pilot study. J Am Osteopath Assoc. 1998;98:155-160.
Dery MA, Yonuschot G, Winterson BJ. The effects of manually applied intermittent pulsation pressure to rat ventral thorax on lymph transport. Lymphology. 2000;33:58-61.
Valenzuela GJ, Hewitt CW, Graham AD. Angiotensin II infusion increases thoracic duct lymph flow in chronically catheterized sheep. Am J Physiol. 1987;252(5 Pt 2):R853-R858.
Onizuka M, Flatebo T, Nicolaysen G. Lymph flow pattern in the intact thoracic duct in sheep. J Physiol. 1997;503(Pt 1):223-234.
Lindena J, Kupper W, Trautschold I. Enzyme activities in thoracic duct lymph and plasma of anaesthetized, conscious resting and exercising dogs. Eur J Appl Physiol Occup Physiol. 1984;52:188-195.
Schad H, Brechtelsbauer H. Thoracic duct lymph in conscious dogs at rest and during changes of physical activity. Pflugers Arch. 1977;367:235-240.
Institute of Laboratory Animal Resources Commission on Life Sciences.
Guide for the Care and Use of Laboratory Animals. Washington DC: National Academy Press;1996 . NIH Publication No. 85-23. Available at:
http://www.nap.edu/readingroom/books/labrats/. Accessed October 6, 2005.
Wallace E, McPartland JM, Jones JM III, Kuchera WA, Buser BR. Lymphatic system: lymphatic manipulative techniques. In: Ward RC.Foundations for Osteopathic Medicine. 2nd ed. Philadelphia, Pa: Lippincott Williams & Wilkins; 2002:1056-1077.
Gashev AA. Physiologic aspects of lymphatic contractile function: current perspectives [review]. Ann N Y Acad Sci. 2002;979:178-187.