Assessment of the excretion time of electronic capsules placed in the intestinal lumen of cows with cecal dilatation-dislocation, healthy control cows, and cows with left displacement of the abomasum

David J.-A. L. Devaux Clinic for Ruminants, Vetsuisse Faculty, University of Berne, 3012 Bern, Switzerland.

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 DR MED VET
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Markus Lempen Institute for Human Centered Engineering, Berne University of Applied Sciences, 2501 Biel, Switzerland.

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 DIPL EI ING FH
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Esther Schelling Swiss Tropical and Public Health Institute and University of Basel, 4051 Basel, Switzerland.

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 DR MED VET, PhD
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Volker M. Koch Institute for Human Centered Engineering, Berne University of Applied Sciences, 2501 Biel, Switzerland.

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 DR SC ETH
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Mireille Meylan Clinic for Ruminants, Vetsuisse Faculty, University of Berne, 3012 Bern, Switzerland.

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 DR MED VET, PhD, DR HABIL

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Abstract

OBJECTIVE To analyze the transit time from various locations in the intestines of cows with cecal dilatation-dislocation (CDD), healthy control cows, and cows with left displacement of the abomasum (LDA).

ANIMALS 15 cows with naturally occurring CDD (group 1), 14 healthy control cows (group 2), and 18 cows with LDA (group 3).

PROCEDURES 5 electronic transmitters were encased in capsules and placed in the lumen of the ileum, cecum, proximal portion of the colon, and 2 locations in the spiral colon (colon 1 and colon 2) and used to measure the transit time (ie, time between placement in the lumen and excretion of the capsules from the rectum). Excretion time of the capsules from each intestinal segment was compared among groups.

RESULTS Cows recovered well from surgery, except for 1 cow with relapse of CDD 4 days after surgery and 2 cows with incisional infection. High variability in capsule excretion times was observed for all examined intestinal segments in all groups. Significant differences were detected for the excretion time from the colon (greater in cows with CDD than in healthy control cows) and cecum (less in cows with LDA than in cows of the other 2 groups).

CONCLUSIONS AND CLINICAL RELEVANCE The technique developed to measure excretion time of capsules from bovine intestines was safe and reliable; however, the large variability observed for all intestinal segments and all groups would appear to be a limitation for its use in assessment of intestinal transit time of cattle in future studies.

Abstract

OBJECTIVE To analyze the transit time from various locations in the intestines of cows with cecal dilatation-dislocation (CDD), healthy control cows, and cows with left displacement of the abomasum (LDA).

ANIMALS 15 cows with naturally occurring CDD (group 1), 14 healthy control cows (group 2), and 18 cows with LDA (group 3).

PROCEDURES 5 electronic transmitters were encased in capsules and placed in the lumen of the ileum, cecum, proximal portion of the colon, and 2 locations in the spiral colon (colon 1 and colon 2) and used to measure the transit time (ie, time between placement in the lumen and excretion of the capsules from the rectum). Excretion time of the capsules from each intestinal segment was compared among groups.

RESULTS Cows recovered well from surgery, except for 1 cow with relapse of CDD 4 days after surgery and 2 cows with incisional infection. High variability in capsule excretion times was observed for all examined intestinal segments in all groups. Significant differences were detected for the excretion time from the colon (greater in cows with CDD than in healthy control cows) and cecum (less in cows with LDA than in cows of the other 2 groups).

CONCLUSIONS AND CLINICAL RELEVANCE The technique developed to measure excretion time of capsules from bovine intestines was safe and reliable; however, the large variability observed for all intestinal segments and all groups would appear to be a limitation for its use in assessment of intestinal transit time of cattle in future studies.

Clinical features of CDD, a common and economically important abdominal disorder that affects primarily dairy cattle, have been described.1–5 In Switzerland, similar prevalences have been observed for CDD and LDA (0.05% at the individual cow level).6 Clinical signs of CDD include a moderate reduction in general condition, a distinct decrease in milk yield, inappetence, decreased or absent ruminal motility, and mild signs of colic, typically with heart and respiratory rates and rectal temperature within reference limits. More specific signs of CDD include positive results for succussion or percussion during auscultation in the right flank combined with detection of a dilated cecum during transrectal palpation. Transrectal palpation findings provide a conclusive clinical diagnosis in 95% of cases. Surgical and medical therapeutic methods have been described for CDD in cattle.7–10 Despite a fair prognosis, recurrence rates are as high as 10% during the first week after surgery.7,11,12 Although the clinical aspects of CDD have been described, pathogenesis of the disease remains poorly understood. Therefore, adequate recommendations for prevention of the disease remain elusive.

Atony or dysmotility of the cecum leading to accumulation of gas and ingesta followed by dilatation and secondary displacement has been suspected as the primary mechanism for the pathogenesis of CDD.3,4,7 However, a myoelectric study13 in cows with delayed recovery or recurrence after surgery for correction of CDD did not reveal a reduction, but rather an increase in the activity of the cecum and proximal portion of the colon in comparison with results for cows with uneventful recovery after CDD and healthy control cows. Because the pattern of myoelectric activity in the cecum and proximal portion of the colon in cows with delayed recovery or relapse after CDD was similar to the pattern usually seen orad to a site of obstruction, a primary motility disturbance in the spiral colon was suspected as the cause of CDD.13,14

Myoelectric patterns in the spiral colon of healthy cows have been described and can be used as a basis for comparison with myoelectric activity in cattle with CDD.15 In 1 study,16 myoelectric patterns recorded by the use of retrievable electrodes in the ileum and large intestine of 8 cows with CDD during the first 4 days after corrective surgery were compared with those recorded in the intestines of 6 healthy control cows. In control cows, physiologic myoelectric activity was recorded in all intestinal segments on all days after surgery. Apparently normal myoelectric activity was evident in the ileum of CDD-affected cows on the first day after surgery, but myoelectric activity patterns in the cecum, proximal portion of the colon, and spiral colon were variable with no organized cyclic myoelectric patterns, with incomplete or normally organized migrating myoelectric complexes, and with a slow return to normal patterns over several days. Despite abnormal myoelectric patterns, all cows had uncomplicated recoveries after CDD. Because there was no relapse of CDD during the 4 recording days, no additional information was gained on the activity of the large intestine during the development (or relapse) of CDD. Although the use of temporary electrodes to record myoelectric activity in the intestines of cattle is an established method for use in research animals as well as in clinical patients,13,16 it remains an invasive and labor-intensive procedure and it may be difficult to obtain owner consent for inclusion of patients in clinical studies.

The objective of the study reported here was to develop a less invasive technique for transit time measurements for use in studies on motility disturbances of the intestines of cattle. In addition, to further explore the pathogenesis of CDD, the transit time between various parts of the intestine (ileum, cecum, PLAC, and spiral colon) and rectum was investigated in cows with CDD and control cows. We hypothesized that comparing the transit times from the various intestinal segments among groups would allow determination of that portion of the intestines with a motility disorder that would lead to the accumulation of gas and ingesta and eventually CDD. Localizing the origin of the motility disorder that causes CDD to a specific segment of the bovine large intestine would constitute a major advance in understanding the pathogenesis of the disease and would allow for further investigations regarding the development, treatment, and prevention of CDD to be focused on the intestinal segment of interest.

Materials and Methods

COWS

Forty-seven cows were included in the study; cows were distributed in 3 groups. Group 1 was composed of 15 dairy cows admitted to our university veterinary clinic because of CDD that required surgical correction. Cattle with concomitant diseases were excluded from the study. Group 2 comprised 14 dairy cows purchased specifically for this study. Those cows (negative control group) were considered healthy on the basis of results of a complete clinical examination and hematologic analysis, including a CBC and a glutaraldehyde test; each cow had a minimal daily milk yield of 20 L. Group 3 consisted of 18 cows with LDA admitted to our university veterinary clinic for surgical treatment. Cows eligible for inclusion in this group had to be > 1 week after parturition and could have no postpartum diseases (eg, retained fetal membranes, metritis, hypocalcemia, or acetonemia) or any other serious pathological changes.

HOUSING AND ANIMAL CARE

All cows were housed in tie-stalls on sawdust bedding. A ration of hay and concentrate calculated for each cow on the basis of body weight and milk yield was distributed over 4 feedings/d. Cows had ad libitum access to water and were milked twice each day. A detailed clinical examination of the animals with emphasis on general condition, appetite, gastrointestinal activity, results of transrectal examination, fecal output and consistency, and milk yield was performed daily.

The study complied with Swiss legislation on animal protection and was approved by the competent Committee for Animal Care and Protection (authorization No. BE3/10). Written owner's consent was obtained for the cows in groups 1 and 3. As mentioned previously, group 2 cows were purchased specifically for the study.

ELECTRONIC DEVICES AND RECORDING OF TRANSIT TIME

A novel system to record intestinal transit time in adult cows was specifically designed for this study. The system, designed in collaboration with the Institute of Human Centered Engineering of the Berne University of Applied Sciences, was based on a radiofrequency system with a transmitter and receiver. The electronic devices were composed of a microcontroller,a transmitter,b and built-in temperature sensor.c For placement in the lumen of a cow's intestines, they were assembled in watertight screw-top capsules (6 × 18 mm) made of polyoxometalate.d An ethylene propylene diene monomer rubber O-ringe was used to help ensure the capsules were watertight. The energy required for the transmitter was provided by two 1.55-V silver oxide batteriesf (Figure 1). Each assembled capsule weighed 2 g.

Figure 1—
Figure 1—

Photograph of the components of an electronic device for recording excretion time in the intestines of cattle. The device consisted of a screw top (A), O-ring (B), capsule (C), battery (D), and radiofrequency transmitter (E). The assembled capsule (F) is also shown.

Citation: American Journal of Veterinary Research 76, 1; 10.2460/ajvr.76.1.60

The receiver was based on an electronic module with a connected preamplifier,g filter,h and appropriate antenna.i Information that included the capsule's identification and measured temperature was transmitted by each capsule every 3 seconds via the receiver to custom-designed software on a personal computer. The data were recorded by the software in a spreadsheetj for each intestinal location, and excretion time was calculated automatically for each capsule.

Conventional steam sterilization of the capsules was not possible because of the batteries; therefore, the capsules were placed in a disinfectant solutionk for 15 minutes prior to surgical placement in the intestines. Transmitters were turned on within 1 hour before surgical placement. Excretion time was defined for each capsule as the time interval from placement into the intestinal lumen (with manual recording of the time of placement in the intestines) until the temperature in the capsule decreased to < 36°C (ie, from placement in the intestinal lumen until the capsule had been excreted from the cow's rectum). A temperature decrease to < 36°C was signaled by an alarm (both auditory and visual [flash of light]), which allowed for recovery of a capsule immediately after it was excreted from a cow's rectum.

SURGICAL PROCEDURES AND POSTOPERATIVE CARE

Cows in group 1 underwent surgery immediately after initial physical examination and confirmation of the diagnosis of CDD and exclusion of concomitant diseases. Preoperative treatment consisted of IV administration of fluids (20 L of isotonic KCl-NaCl solution), oxytetracycline (10 mg/kg), and flunixin meglumine (2.2 mg/kg). Cows were restrained in a standing position, and regional anesthesia (paravertebral nerve block achieved through infiltration of 2% lidocaine hydrochloride)17 was provided. Routine laparotomy was performed. The position of the cecum, PLAC, and spiral colon in the abdomen was recorded. The apex of the cecum was exteriorized, and cecal and colonic contents were drained as described elsewhere.18 The typhlotomy site was closed, and the cecum was repositioned. Then, final exploration of the abdominal cavity was performed. Five intestinal segments of interest were exteriorized (ileum, cecal body, PLAC, and 2 locations in the spiral colon [second outermost centripetal loop {colon 1} and third outermost centrifugal loop {colon 2}]; Figure 2). A short (≤ 1 cm) enterotomy incision was made in each of these intestinal segments, and a capsule containing an electronic transmitter was placed in the lumen of each segment. Each of the 5 incisions was closed in 2 layers with polyglyconate 3–0.l A cruciate interrupted suture was initially placed to rapidly close the lumen, which was followed by oversewing with a Cushing suture. In the spiral colon, the serosa was incised prior to enterotomy; the intestinal wall was sutured as described, which was followed by suturing the serosa with polyglyconate 3–0 in a simple continuous pattern. The abdominal cavity was closed in a routine manner.19

Figure 2—
Figure 2—

Schematic illustration of the sites for placement of electronic capsules in the lumen of the ileum (A), cecum (B), PLAC (C), second outermost centripetal loop of the spiral colon (colon 1; D), and third outermost centrifugal loop of the spiral colon (colon 2; E) in dairy cattle.

Citation: American Journal of Veterinary Research 76, 1; 10.2460/ajvr.76.1.60

For cows of group 2, feed was withheld for 24 hours prior to surgery to mimic the reduction in feed intake associated with inappetence caused by CDD. Cows of group 2 underwent the same surgical procedure as the cows of group 1, including enterotomy at the cecal apex and drainage of contents of the cecum and large intestine, which was followed by placement of an electronic capsule in each of the 5 intestinal locations.

Cows of group 3 underwent similar procedures after initial examination to confirm the diagnosis of LDA and exclusion of concomitant diseases. Laparotomy was performed via the right flank to enable repositioning of the abomasum and omentopexy.20 Prior to closure of the abdominal wall and omentopexy, the cecal apex was exteriorized and cecal contents were drained. The 5 transmitters were placed in the intestinal lumen as in groups 1 and 2.

Postoperative care of all cows included administration of isotonic KCl solution (15 L, PO, immediately after surgery), oxytetracycline (5 mg/kg, IV, q 12 h for 4 days), and isotonic KCl-NaCl solution (20 L, IV) as well as administration of 2 L of fresh ruminal fluid with 15 L of isotonic KCl solution via orogastric tube once on the first day after surgery. Feed was withheld from all cows for 24 hours after surgery. Cows were subsequently fed restrictively, and feed was slowly reintroduced as follows: on days 1, 2, 3, and 4, each cow was offered 25%, 50%, 75%, and 100% of the calculated ration, respectively. The amount of uneaten feed was recorded.

After all 5 electronic capsules were excreted, postoperative treatment was completed, and postoperative recovery of the cows was considered to be satisfactory, cows of groups 1 and 3 were discharged to their owners. Cows of group 2 were sent to slaughter after an appropriate withdrawal time.

DATA ANALYSIS

In addition to excretion time recorded by the recording system for each location (ie, between the location of the capsule in the intestine and excretion from the rectum), a virtual transit time between the various intestinal locations was calculated by subtracting the excretion time for the distal location of interest from the excretion time for the proximal location of interest (ie, virtual transit times between the ileum and cecum, cecum and PLAC, PLAC and colon 1, and colon 1 and colon 2 were calculated). Because the excretion sequence did not always correspond to the expected pattern based on the anatomic location of capsule placement, negative values were obtained for some of the calculated virtual transit times. Negative values for the calculated virtual transit times between placement locations were not considered in the statistical analysis.

STATISTICAL ANALYSIS

Measured transit time and virtual transit time of each intestinal segment were compared among groups with the Kruskal-Wallis test by use of statistical software.m Values were considered significant at P ≤ 0.05. Multiple pairwise comparisons were performed by use of the Dunn test and Bonferroni-adjusted P values.n

Results

COWS AND CLINICAL FINDINGS

All cows were of the common Swiss dairy breeds. The study included 26 Simmental–Red Holstein crossbreds, 13 Holsteins, 3 Red Holsteins, 2 Simmentals, and 3 Brown Swiss. Group 1 consisted of 7 Simmental–Red Holstein crossbreds, 5 Holsteins, 2 Red Holsteins, and 1 Brown Swiss. Group 2 consisted of 7 Simmental–Red Holstein crossbreds, 3 Holsteins, 2 Simmentals, and 2 Brown Swiss. Group 3 consisted of 12 Simmental–Red Holstein crossbreds, 5 Holsteins, and 1 Red Holstein. Age of cows was comparable in all groups (mean of 4.5, 3.3, and 3.8 years for groups 1, 2, and 3, respectively).

All 15 cows of group 1 had been referred to our university veterinary clinic because of a tentative diagnosis of CDD. Cows of this group had signs of disease for a mean of 1.3 days before referral. They all had a reduction in general condition, with rectal temperature and heart and respiratory rates within reference limits. Fecal output was reduced for 9 cows and was not evident for the other 6 cows. Succussion and percussion during auscultation of the right flank yielded positive results in all but 1 cow. Only 2 cows had signs of colic. The definitive diagnosis of CDD was confirmed by transrectal examination in all cows; retroflexion of the cecum was detected in 6 cows.

All cows of group 2 were healthy. Health status was confirmed on the basis of results of clinical examinations and hematologic analysis.

For group 3, 15 cows had been referred to our university veterinary clinic because of suspected LDA, 1 cow because of suspected right displaced abomasum, 1 cow because of suspected CDD, and 1 cow because of suspected CDD or LDA. Cows of this group had signs of disease for a mean of 2.7 days before referral. Diagnosis of LDA was confirmed by a positive result for succussion and percussion during auscultation of the left flank in all cows. Concomitant diseases were ruled out on the basis of results of clinical examinations and hematologic analysis.

SURGICAL FINDINGS AND SHORT-TERM RECOVERY

All cows, except for 1, remained in standing position throughout surgery. One cow with CDD lay down after typhlotomy; the surgery was continued with the cow in left lateral recumbency without further complications.

Of the 15 cows of group 1, 8 had a simple dilation of the cecum, 6 had cecal retroflexion, and 1 had a cecal torsion. Ingesta contained in the cecum were liquid to soft in all cows, except 1 cow that had cecal contents that were distinctly more dry. The cecal wall remained mainly atonic without signs of contraction after typhlotomy. Complete exploration of the abdominal cavity did not reveal other abnormalities in the cows of group 1.

The healthy control cows of group 2 appeared to be more agitated than those of group 1 during paravertebral anesthesia, but no other differences from cows of group 1 were noticed during surgery, except that it was easier to exteriorize the cecum. For all cows of group 3, the abomasum was still displaced to the left side at the time of surgery. No other differences were noticed in comparison with the cows of group 2.

Capsules could be placed into the intestinal lumen without major difficulties. In a few instances, small amounts of ingesta leaked from the enterotomy site after incision of the intestinal wall, mostly during placement of capsules in the colon. Any leaked intestinal content was immediately removed, and the intestinal wall was cleaned with moisturized sterile sponges. No further complications were recorded.

During the recovery period, 1 cow of group 1 had a reduction in general condition on postoperative day 4, which was after the 2 capsules placed in the spiral colon had been excreted. Transrectal examination revealed a distinctly dilated cecal apex. Serum biochemical analysis revealed only a slight reduction of the total serum calcium concentration (1.98 mmol/L; reference range, 2.0 to 3.0 mmol/L). The cow was treated successfully with an IV infusion of calcium gluconate (500 mL of a 200 mg/mL solution) and sodium sulfate (200 g, PO) as a purgative. One cow of group 3 had an increase in rectal temperature and reduction in general condition on day 4 after surgery, which was after all capsules had been excreted. Clinical examination of that cow revealed moderate amounts of malodorous uterine discharge (endometritis). The endometritis was treated with a single injection of prostaglandin and resolved within 2 days. In addition, 1 cow from group 3 developed severe indigestion 2 days after surgery, which was after excretion of all capsules; this cow recovered fully after being treated by administration of fresh ruminal juice for several days. Finally, one cow of group 1 and another cow of group 2 developed an incisional infection with subsequent abscess formation, which became evident in the cow of group 1 at 3 days after surgery and in the cow of group 2 at 10 days after surgery. In both cows, all capsules had been excreted at the time the incisional infection became evident. These 2 cows had no other complications after surgery and did not have alteration of their general condition. In both cows, enlargement of the wound area was palpably evident in the right flank, transabdominally, and during transrectal examination. Transcutaneous and transrectal ultrasonographic examination of the enlargement indicated abscess formation. The cow of group 1 was slaughtered after treatments were unsuccessful. The cow of group 2 was not treated and was sent to slaughter. All remaining cows recovered well from surgery.

TRANSIT TIME

The electronic recording system functioned well in most cows and allowed for determination of the time of excretion from all intestinal locations in most animals. However, because of technical problems with the transmitters, antenna, recording software, or computer, the data set was not complete for 3 cows (2 in group 1, both of which had missing values for the ileum, cecum, and PLAC; and 1 in group 2, which had a missing value for the PLAC). Data for a cow in group 1 that received additional treatment because of relapse of CDD and for 2 cows (one in group 1 and the other in group 2) with incisional abscesses were not included in the statistical analyses.

Median excretion time for all groups (excluding the cow with CDD relapse and the 2 cows with incisional abscesses) was 18.8 hours from the ileum, 19.3 hours from the cecum, 14.1 hours from the PLAC, and 7.2 and 6.4 hours from the proximal and distal location in the spiral colon, respectively (Table 1). Most cows (42/44) excreted all capsules within 5 days. Only 2 cows had considerably greater excretion times; one (in group 1) excreted the last capsule (from the PLAC) after 7 days, and the other (in group 2) excreted the capsule placed in the ileum after 10 days. For 2 of the 41 cows with a complete data set (both in group 3), the difference between the first and last excreted capsule was < 40 minutes, and for 7 cows (3 in group 1, 2 in group 2, and 2 in group 3), the excretion time of the last excreted capsule was more than twice as long as the transit time of the preceding capsule, independent of the excretion sequence of the capsules.

Table 1—

Excretion time (minutes) between placement of an electronic capsule in various intestinal segments and excretion from the rectum for 13 dairy cows with CDD (group 1), 13 healthy control cows (group 2), and 18 cows with LDA (group 3).*

LocationGroup 1Group 2Group 3
Ileum1,296.5 (651–2,935)1,645.0 (1,093–2,033)841.5 (623–1,353)
Cecum1,984.0 (978–2,499)a1,434.0 (1,130–2,849)a796.5 (633–1,393)b
PLAC1,108.5 (446–1,915)937.0 (727.5–1,202.5)748.0 (662–1,110)
Colon 1480.0 (399–683)343.0 (167–497)461.5 (201–688)
Colon 2668.0 (469–983)c242.0 (204–385)d378.5 (257–524)c,d

Values reported are median (IQR).

Data from 3 additional cows (1 in group 1 with relapse of CDD, and 1 each in group 1 and group 2 with incisional infection) were excluded from analysis.

Colon 1 = Proximal location in the spiral colon (second outermost centripetal loop). Colon 2 = Distal location in the spiral colon (third outermost centrifugal loop).

Within a location, values with different superscript letters differ significantly (P ≤ 0.05).

Within a location, values with different superscript letters differ significantly (P ≤ 0.01).

The excretion time did not always reflect the actual distance between the site of placement in the intestines and the rectum of the cows (ie, the capsule placed in the distal location of the spiral colon was not always the first to be excreted, and the capsule placed in the ileum was not always the last to be excreted). Sixteen patterns of excretion sequence were observed (Table 2). Only the 41 cows with complete data sets for all 5 capsules were considered for the determination of the excretion sequence; cows with missing values were excluded. No systematic differences in the excretion sequence were evident among groups. The most frequently observed sequence was colon 1, colon 2, PLAC, cecum, and ileum in 10 cows and colon 1, colon 2, PLAC, ileum, and cecum in 7 cows. The anatomically expected excretion sequence of colon 2, colon 1, PLAC, cecum, and ileum was observed in 2 cows. Ten of the 16 sequences were observed in 1 cow each. Variation in the excretion sequences was most pronounced between the ileum and cecum and between colon 1 and colon 2. The capsule placed in the cecum was the last to be excreted in 19 of 41 cows, whereas the last capsule excreted was the one placed in the ileum in 14 cows. In the remaining 8 cows, another capsule was the last one excreted (the capsule placed in the PLAC in 7 cows and the capsule placed in colon 1 in 1 cow).

Table 2—

Number of cows in each of 3 groups* that had a specific sequence of excretion for 5 capsules placed in the intestinal lumen at various locations.

Excretion orderGroup 1Group 2Group 3Total
5, 4, 3, 2, 11102
5, 4, 3, 1, 21225
5, 4, 1, 3, 20011
5, 4, 1, 2, 31045
4, 5, 3, 2, 115410
4, 5, 3, 1, 20257
4, 5, 2, 3, 10101
4, 5, 2, 1, 30011
4, 5, 1, 2, 30101
4, 5, 1, 3, 20011
5, 1, 3, 4, 21001
5, 3, 4, 2, 11001
4, 1, 3, 5, 22002
3, 5, 4, 1, 21001
2, 1, 3, 5, 41001
1, 3, 5, 4, 21001

Data from 11 cows in group 1, 12 cows in group 2, and 18 cows in group 3; data from 3 cows (1 in group 1 with relapse of CDD, and 1 each in group 1 and group 2 with incisional infection) were excluded from this analysis, as well as data from 3 additional cows (2 in group 1 and 1 in group 2) for which data were missing from one or several intestinal locations.

1 = Ileum. 2 = Cecum. 3 = PLAC. 4 = Proximal location in the spiral colon (second outermost centripetal loop). 5 = Distal location in the spiral colon (third outermost centrifugal loop).

The difference in excretion time between the ileum and cecum was < 15 minutes in 14 of 41 cows; in 8 of these 14 cows, the capsule that had been placed in the cecum was excreted last. Thirty-four of 41 cows excreted the 2 capsules placed in the colon first, but the capsule placed in colon 1 was excreted prior to that placed in colon 2 in 21 of these 34 cows. In 20 cows, the difference between colon 1 and colon 2 was < 15 minutes; in 13 of these cows, the capsule placed in the proximal portion of the spiral colon was excreted before the one placed in the distal portion of the spiral colon.

Because errors in the anatomic location of the placement sites in the spiral colon could not be excluded with absolute certainty (ie, placement of the colon 1 capsule in a more distal location than placement of the colon 2 capsule as a result of erroneous identification of the various loops of the spiral colon during surgery), evaluation of the excretion time was also repeated with a single value for the colon consisting of the mean for colon 1 and colon 2. Ten excretion sequences were recorded with a single mean value for the spiral colon. The most common excretion patterns (in 12 cows each) were colon, PLAC, cecum, and ileum (ie, the anatomically expected sequence) and colon, PLAC, ileum, and cecum. Three other excretion patterns were observed in 6 cows, 4 cows, and 2 cows, respectively, and 5 cows each had a separate excretion sequence.

Additional statistical analyses were conducted after exclusion of the negative calculated transit time values between adjacent intestinal segments that resulted from variation in excretion sequences.

A high degree of variability in the excretion time duration was observed for all groups (Table 1). Significant differences among groups were observed for the measured time between capsule placement in the cecum and excretion from the rectum, whereby the excretion time was significantly (P ≤ 0.05) less for group 3 than for groups 1 and 2 (Figure 3), and between capsule placement in colon 2 and excretion from the rectum (P ≤ 0.01), in which the excretion time was significantly (P ≤ 0.01) greater for group 1 than group 2, whereas the difference was not significant (P = 0.06) between group 1 and group 3 (Figure 4). There was also a significant (P = 0.018; Kruskal-Wallis test) difference when the mean value for both locations in the spiral colon was used. The excretion time was significantly (P = 0.007) greater for group 1 (median, 579.0 minutes; IQR, 463 to 707.5 minutes) than for group 2 (median, 346.5 minutes; IQR, 188.5 to 416.5 minutes). The excretion time for group 1 and group 3 (median, 426.2 minutes; IQR, 228 to 591 minutes) did not differ significantly (P = 0.11). For the calculated virtual transit times, a significant (P = 0.037) difference was found only for the cecum-PLAC segment among group 1 (median, 532.0 minutes; IQR, 152 to 985 minutes), group 2 (median, 522.0 minutes; IQR, 202 to 2,918 minutes), and group 3 (median, 23.0 minutes; IQR, 17 to 227 minutes), whereas there were no significant differences detected by use of pairwise comparisons.

Figure 3—
Figure 3—

Box-and-whisker plots of excretion time between placement in the cecum and excretion from the rectum for 13 dairy cows with CDD (group 1), 13 healthy control cows (group 2), and 18 cows with LDA (group 3). Data for 3 additional cows (1 in group 1 with relapse of CDD, and 1 each in group 1 and group 2 with incisional infection) were excluded from analysis. For each plot, the box represents the IQR, the horizontal line in each box represents the median, and the whiskers represent the range of values within a value of the upper or lower limit of the box ± (1.5 × [upper or lower limit of the box – median]). a,bValues with different superscript letters differ significantly (P ≤ 0.05).

Citation: American Journal of Veterinary Research 76, 1; 10.2460/ajvr.76.1.60

Figure 4—
Figure 4—

Box-and-whisker plots of excretion time between placement in the third outermost centrifugal loop of the spiral colon (colon 2) and excretion from the rectum (A) and mean excretion time between placement in the 2 locations in the spiral colon (colon 1 and 2) and excretion from the rectum (B) for 3 groups of cows. See Figure 3 for remainder of key.

Citation: American Journal of Veterinary Research 76, 1; 10.2460/ajvr.76.1.60

A cow in group 1 excreted both capsules from the spiral colon prior to relapse of CDD. Excretion times for colon 1 and colon 2 were 440 and 555 minutes, respectively, which were comparable to the median excretion times observed in the other cows of all groups. In contrast, the transit times for the ileum (10,534 minutes) and PLAC (10,844 minutes) were in the upper quartiles of the values observed in the other cows of all groups. The value for the cecum was missing for that cow.

Discussion

To the authors’ knowledge, the study reported here represented the first report of the use of electronic transmitters for the assessment of transit time in cattle. This technique has been described in humans, dogs, and ponies.21,22 Because of the size of adult cattle and because of the costs associated with the commercially available recording systems, which are prohibitive for food animals, the development of a novel device to measure the transit time in cows was necessary. A measurement system based on radiofrequency technology was designed and tested, with successful results, on 3 healthy control cows prior to the start of the present study. In the course of the experiments, however, several technical problems led to dysfunction of the system and subsequent loss of data. The encountered disturbances included computer shutdown (recordings made in the barn were affected because dust impaired the computer cooling system and caused overheating), software and antenna dysfunction, and corrosion of the contact points between the radiofrequency transmitter and battery in the capsules. For these reasons, the system was reviewed and improvements made periodically. Major changes included the acquisition of a dust-resistant computer, use of galvanized contact points, improvements in varnishing of the electronic devices, and an extensive examination of the entire system after every fifth measurement. With these improvements, the system became a reliable tool for use in measuring excretion time of the capsules from the intestines of adult cattle. However, some data were lost in the process because of missing values or incomplete measurements.

Regarding the surgical procedures, the only differences among groups were that the healthy control cows appeared to be more agitated during paravertebral anesthesia and the cows with CDD had more signs of pain during exteriorization of the cecum. There were no differences among groups with regard to the other surgical manipulations and placement of the capsules. Mean time needed for implantation of the 5 capsules did not exceed 45 minutes for all groups. Two of 47 cows developed signs of incisional infection several days after surgery. For these 2 cows, the immediate postoperative recovery was considered uncomplicated and all capsules were excreted before the cows had onset of signs of illness. Some contamination had occurred during surgery in both cows (extended duration of surgery in the cow of group 1 and contamination of the incision as a result of unruly behavior at the end of surgery in the cow of group 2). Nevertheless, the observed incisional infection rate (2/47 [4.3%]) was not higher than the value of 4.3% reported for surgeries performed in clean hospital facilities.23 Results from these 2 cows were excluded from all analyses on the basis that incisional infection had likely begun at the time of surgery and may have influenced intestinal tract activity and excretion time of the capsules in these 2 cows, despite the fact that the infection became clinically evident only several days later. Two other cows were readmitted to our veterinary clinic 1 month and 19 months after surgery, with relapse of CDD and recurrence of LDA, respectively. Both underwent a second corrective surgery, but no signs of the preceding surgery were observed in the abdominal cavity or in the intestinal wall at the sites of capsule placement during laparotomy. On the basis of these anecdotal observations and because of the uneventful course of recovery recorded for almost all cows in the study, we believe that the surgical technique used for capsule placement can be considered safe.

One of 15 cows with CDD had recurrence of the condition 4 days after surgery, which is in agreement with the reported relapse rate of 10% during the postoperative phase.12 Only 2 capsules (colon 1 and colon 2) had been excreted at the time of CDD relapse, both of which were excreted within 10 hours after surgery (7 and 9 hours, respectively). The remaining capsules placed in the ileum and PLAC were excreted after 7 days (7.3 and 7.5 days, respectively), which correlated with resolution of the relapse and restoration of fecal output. The value for the capsule placed in the cecum was missing for this cow. It is not possible to determine, on the basis of results for a single cow with CDD relapse, whether the pattern observed indicated that the motility disorder leading to CDD was located in the proximal portion of the spiral colon or whether other systemic factors, such as hypocalcemia, after excretion of the capsules from the spiral colon caused recurrence of CDD. Indeed, another cow from group 1 had a similar pattern with a short excretion time for the capsules placed in the spiral colon (480 and 469 minutes for colon 1 and 2, respectively) and distinctly greater excretion times for the other 3 capsules (6.7 days for the ileum, 6.8 days for the cecum, and 6.8 days for the PLAC). This cow did not have clinical signs of CDD relapse or other abnormalities during the recovery period.

Except for surgery, controlled feeding, and fluid administration, no other supportive treatments, such as administration of prokinetic drugs or purgatives,24 were provided for cows with CDD. Nevertheless, the short-term recovery rate in the present study was congruent with the recurrence rate of 10% described in the literature.7,11 Similar results have been observed in another study16 in which investigators used the same protocol for preoperative and postoperative treatment in cows with CDD and myoelectric measurements were obtained. Despite the limited number of animals included in these reports, this observation leads to questions about the essential aspects of conservative and postoperative treatment of CDD. The authors are not aware of any prospective study conducted to compare the effects of various treatment regimens for CDD.

Distribution of the breeds of cattle involved in the present study was representative of the breed distribution of patients in our veterinary clinic, and no obvious breed differences were evident between the CDD and LDA groups. An increased frequency of CDD in Brown Swiss and of LDA in Holsteins, as reported previously,6 was not evident in the patients of the present study, possibly because of the small number of cows in each group.

The main purpose of the study reported here was to measure the transit time from various locations in the distal portion of the small intestines and proximal portion of the large intestine and to compare values for cows with CDD against those for a negative control group (healthy cows) and those for a positive control group (cows with another motility dysfunction in the digestive tract [ie, LDA]). Comparison of results for the 3 groups was expected to provide insights into the location of the primary motility disturbance that leads to CDD. Results of previous studies13,16 suggest that the spiral colon is the primary site for the origin of CDD; therefore, the transmitter-containing capsules were placed in intestinal segments orad to the spiral colon (ileum, cecum, and PLAC) as well as 2 locations in the spiral colon.

Analysis of the measurements revealed a large variability in excretion time of the capsules from all intestinal segments in all groups of cows. Excretion time from the ileum and cecum in the 3 groups ranged from 4 to > 200 hours, for the PLAC ranged from 6 to > 160 hours, and for the spiral colon ranged from 1 to > 30 hours. In addition, the excretion sequence of the capsules was not consistent (ie, capsules placed in the most distal intestinal segments were not always excreted first). In all groups, the main irregularities in the excretion sequence were between the ileum and cecum and between colon 1 and colon 2. Excretion of the capsule placed in the ileum prior to excretion of the one placed in the cecum can likely be explained by the fact that the capsule in the ileum may have been transported directly from the ileocecal junction to the PLAC, thus bypassing the cecum and reaching the rectum sooner than the capsule placed in the cecum. In contrast, variation in the excretion sequence of the capsules placed in a proximal and distal loop of the spiral colon cannot be explained by a bypass effect in the tubular structure of the colon. One possible reason for a more rapid transit of a capsule might have been related to the consistency of the colonic contents, given that a capsule placed in an intestinal segment containing more solid ingesta might have been transported more efficiently than a capsule placed within liquid ingesta. Differences in intestinal transit time have been described for liquid and solid phases by use of scintigraphic evaluations in ponies.25 We did not detect an association of specific excretion patterns with recorded fecal consistency in the present study (data not shown); however, the fact that bovine feces are generally of lesser and more variable consistency than are feces of other species in which similar methods for assessment of transit time have been described (dogs and ponies)21,22 may explain the greater variability of the results obtained in cattle. Alternatively, there might have been an error in the identification of the second outermost centripetal loop and third outermost centrifugal loop of the spiral colon during surgery, which could have led to placement of the capsule for colon 2 in a more proximal location than the capsule for colon 1. This scenario cannot be excluded with certainty in all cases because it may be difficult to exteriorize the spiral colon and identify its loops, especially if the colon is distended as in cows with CDD or in cattle with large amounts of fat in the colonic mesentery. The fact that excretion of the capsule for colon 1 prior to excretion of the capsule for colon 2 was observed in all groups indicated that difficulties attributable to distention of the colon in cows with CDD likely did not lead to inaccurate identification of the placement sites in cows with CDD. However, to rule out a potential effect of erroneous placement of the colonic capsules, all statistical analyses were repeated with a mean for the excretion time of both spiral colon locations, which eliminated potential variability associated with such an error. The repeated analyses yielded similar results as for the analyses with the original data; thus, differences among groups for the transit time from the colon were believed to be valid, even if an error should have happened with regard to the placement sites in the spiral colon locations in a few cows. An error in the anatomic location for capsule placement was not possible for the other locations, which could be identified without doubt; thus, the large degree of variability observed in the excretion sequence of the capsules was believed to be an actual feature associated with this method for measurement of transit time in the bovine intestines.

A significant difference among groups was observed for the excretion time from the cecum as well as for the calculated transit time between the cecum and PLAC. The excretion time from the cecum was significantly less in cows with LDA (group 3) than in the other 2 groups of cows. For the calculated transit time between the cecum and PLAC, there was a significant difference detected by use of the Kruskal-Wallis test, but no significant differences were evident for the pairwise comparisons, although the calculated transit time for cows with LDA (group 3) was less than that for group 2 (P = 0.069). The latter results suggested intestinal motility was not decreased in the area of the cecum in cows with LDA. This is a contradiction with the authors’ clinical observations during surgery that the cecum is often slightly distended with gas in cows with LDA. This discrepancy may be explained by a rapid reestablishment of physiologically normal motility in the large intestine after correction of LDA.

Statistical analysis also revealed significant (P = 0.009) differences in the transit time from colon 2 among the 3 groups of cows, with a significantly greater transit time for cows with CDD (group 1) than for healthy control cows (group 2), whereas the difference in transit time between cows with CDD and cows with LDA (group 3) was not significant (P = 0.06). The difference between group 1 and group 2 was also significant (P = 0.007) when the analysis was performed with the mean value of both colonic locations. This is in accordance with results of previous studies in which a delayed normalization of motility was observed in the spiral colon after implantation of permanent electrodes in cows under general anesthesia26 as well as after implantation of retrievable electrodes in standing cows undergoing surgery for correction of CDD.16 These findings further support the hypothesis that the origin of the motility disorder that leads to CDD may be located in the spiral colon.

In the study reported here, the method for measurement of the excretion time of capsules placed in the lumen of the intestines of cows was reliable; however, the high variability observed in the excretion times, including irregular excretion sequences for the capsules, may preclude use of this method for assessment of transit time in clinical studies (eg, evaluation of the effects of prokinetic drugs on motility of the large intestine in cattle). The significantly greater excretion time observed for the spiral colon of cows with CDD in comparison with that for healthy control cows, despite the high degree of variability, confirmed the results of other studies whereby it has been suggested that a motility disorder in the spiral colon may play a role in the pathogenesis of CDD.

Acknowledgments

Supported in part by a grant of the Specialization Board of the Vetsuisse Faculty of the University of Berne, Switzerland.

ABBREVIATIONS

CDD

Cecal dilatation-dislocation

IQR

Interquartile range (25th to 75th percentile)

LDA

Left displacement of the abomasum

PLAC

Proximal loop of the ascending colon

Footnotes

a.

Microcontroller, Silicon Laboratories, Austin, Tex.

b.

433-MHz RF transmitter, ISM band (amplitude shift keying modulation), Melexis Technologies NV, Ieper, Belgium.

c.

Temperature sensor, Texas Instruments Inc, Dallas, Tex.

d.

Polyoxometalate-C medical grade, Amsler und Frey, Schinznach-Dorf, Switzerland.

e.

O-ring, EPDM with FDA authorization, Brütsch/Rüegger Werkzeuge AG, Urdorf, Switzerland.

f.

1.55-V silver oxide batteries, Renata Batteries, Itingen, Switzerland.

g.

Amplifier, ZFL, Mini-Circuits, Brooklyn, NY.

h.

SAW filter, EPCOS, München, Germany.

i.

Dipolantenna, ANT-433-MHW, Linx Technologies Inc, Merlin, Ore.

j.

Excel, Microsoft Corp, Redmond, Wash.

k.

Desomedan, Desomed Dr. Trippen GmbH, Freiburg, Germany.

l.

Monocryl, Ethicon, Johnson & Johnson, New Brunswick, NJ.

m.

Stata/IC, version 12, Stata Corp LP, College Station, Tex.

n.

dunntest, Stata, version 12, Stata Corp LP, College Station, Tex. Available at: www.doyenne.com/stata/dunntest.html. Accessed Jun 10, 2014.

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