J. Dairy Sci.

99:8472–8476
http://dx.doi.org/10.3168/jds.2015-10810
© American Dairy Science Association®, 2016.

Short communication: Iodine concentrations in serum, milk, and tears

after feeding Ascophyllum nodosum to dairy cows—A pilot study
U. S. Sorge,*1 M. Henriksen,† A. Bastan,‡ N. Cremers,§ K. Olsen,§ and B. A. Crooker#
*Department of Veterinary Population Medicine, University of Minnesota, Saint Paul 55108
†Department of Veterinary Clinical Sciences, University of Minnesota, Saint Paul 55108
‡Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, Ankara University, Ankara, Turkey
§Veterinary Diagnostic Laboratory, University of Minnesota, Saint Paul 55108
#Department of Animal Science, University of Minnesota, Saint Paul 55108

ABSTRACT group. Liver mineral profiles were comparable between

groups and generally did not change over the course of
Kelp (Ascophyllum nodosum) is rich in iodine and of- the study. Thyroid hormones remained overall within
ten fed by organic dairy producers as a mineral supple- the reference range throughout the trial. Neither milk
ment to support animal health. A commonly held belief nor tears from kelp-fed cows inhibited in vitro growth
is that kelp supplementation decreases susceptibility to of any of the plated bacteria. In summary, serum iodine
infectious bovine keratoconjunctivitis due to increased concentration was correlated with the iodine concentra-
iodine concentrations in tears. Whereas serum and tion in milk and tears and feeding kelp increased only
milk iodine concentrations are positively correlated the serum iodine levels of cows in this trial. Bacterial
and modulated by oral iodine supplementation, noth- growth was not inhibited in milk and tears of kelp-fed
ing is known about the iodine concentration of tears. cattle in vitro, and prevention of infectious bovine kera-
Therefore, the 3 objectives of this pilot study were to toconjunctivitis would not be based solely on increased
determine (1) the iodine content of tears, milk, and iodine concentrations in tears.
serum of cows after being fed kelp for 30 d; (2) the Key words: tears, iodine, kelp, Ascophyllum nodosum,
trace mineral and thyroid status of cows before (d 0) infectious bovine keratoconjunctivitis
and after being fed kelp for 30 d; and (3) the in vitro
growth rate of bacteria in tears (Moraxella bovis) or
Short Communication
milk (Staphylococcus aureus, Escherichia coli, Strepto-
coccus uberis) collected from cows fed no kelp (d 0) or Organic producers are using different preventive
kelp (d 30). Cows (n = 3/treatment) were individually approaches to support animal health because their
fed 56 g of kelp per day (n = 3/treatment) or not (n = treatment options are limited (AMS, 2015). Feed
3/no treatment) for 30 d. Daily feed intake of the TMR supplementation with kelp (Ascophyllum nodosum), a
was recorded and weekly TMR, kelp, milk, blood and brown seaweed, as a mineral source is practiced by well
tear samples were collected and analyzed for iodine. over 50% of organic dairy producers (Antaya et al.,
The feed samples were pooled and further analyzed for 2015; Sorge et al., 2016). Many organic dairy produc-
other minerals. On d 0 and 30, liver biopsies and blood ers believe that feeding kelp will improve the health of
samples were collected and analyzed for mineral content their animals because kelp is rich in iodine and other
and thyroid hormone concentrations, respectively. An important trace minerals (Antaya et al., 2015). The
inhibition test used milk and tear-soaked plates from positive effect of kelp on health is mostly focused on
kelp-fed cows (d 0 and 30) as well as 1 and 7.5% iodine improved udder health, reproduction, and particularly
as positive and distilled water as negative control. As the prevention of infectious bovine keratoconjunctivitis,
expected, serum iodine concentrations were positively which is also called pink eye (Olree and Dettloff, 2010;
correlated with milk and tear iodine concentrations. Antaya et al., 2015). In particular, the latter observa-
Whereas the iodine concentrations in serum increased tion is explained by the assumption that an increased
significantly in the kelp-fed cows during the 30-d study, concentration of iodine in tears will decrease the growth
milk and tear iodine concentrations increased only of Moraxella bovis or Moraxella bovoculi, the causative
numerically in these cows compared with the control agents of pink eye. However, although feeding kelp in-
deed increases the iodine concentration in hair (Olree
and Dettloff, 2010) and milk of cows (Antaya et al.,
Received December 23, 2015.
Accepted June 11, 2016. 2015), little information is available at present to assess
1
Corresponding author: [email protected] the effect of kelp supplementation on cattle health. The

8472
 SHORT COMMUNICATION: TEAR IODINE CONCENTRATIONS 8473

only existing long-term study supplemented a differ- sian cows were randomly assigned to either the kelp
ent kind of kelp (Macrocystis pyrifera) and the authors (n = 3) or the negative control group (n = 3). The
were unable to find any “consistent differences which cows were fed an individually weighed TMR that was
[could] be attributed to the rations fed. […] The ad- the same for all cows (Table 1). The kelp group was
dition of kelp meal to normal rations for dairy heifers additionally fed 56 g/d of kelp (Kelp, Thorvin, New
showed no particular benefits for growth, breeding effi- Castle, VA) that was manually top dressed and mixed
ciency, general health, physical condition, appetite, and into the TMR at 28 g in the morning and evening feed-
size and condition of calves at birth” (Berry and Turk, ing. The 56 g/d responded to a recommended 0.5% of
1944). To the best of our knowledge, no studies have DMI (E. Chandler, Thorvin, personal communication).
been conducted to validate the effect of feeding kelp on Each morning, the refusal was weighed to estimate the
the incidence of infectious bovine keratoconjunctivitis, daily intake of each cow. Furthermore, each week, a
let alone to measure the iodine concentration in tears. small sample of the kelp fed as well as a grab sample
However, it is well established that iodine is crucial of the TMR were collected and frozen. The weekly kelp
for animal health. Oral iodine supplementation is and TMR samples were combined (separately) for sub-
positively correlated with the iodine concentrations in sequent mineral and iodine analysis.
serum and milk in cows (Schöne et al., 2009) and feed- Blood (10-mL serum Vacutainer, 21-gauge, 1.5-inch
ing iodine-rich kelp increases iodine levels in milk (Rey- needles; BD, Franklin Lakes, NJ,) and tear samples
Crespo et al., 2014; Antaya et al., 2015). Therefore, it were collected weekly from each cow (d 0, 7, 14, 21, and
is probable that the concentration of iodine in serum 30). To collect tears, the head of the cow was restrained
and tears could also be positively correlated. Increased with a halter, the third eye lid of the cow was prolapsed,
iodine concentrations in tears may indeed improve the and a Weck-Cel sponge (Weck-Cel, Merisol, Houston,
animal’s ability to cope with M. bovis infections, just TX) was gently held into the medial corner of the cow’s
as increased iodine levels in the upper respiratory tract eye to absorb approximately 1 mL of tear fluid per eye
contributed to airway antiviral defenses (Derscheid et in the morning and afternoon after the cows returned
al., 2014). Therefore, the 3 objectives of this pilot study from milking. The sponge was placed into a 2.5-mL Ep-
were to determine (1) the iodine content of tears, milk, pendorf tube with microfilter and centrifuged at 3,000
and serum of cows after being fed kelp (56 g/d) for × g for 20 min at 20°C.
30 d; (2) the trace mineral and thyroid status of cows
before (d 0) and after being fed kelp for 30 d; and (3)
Table 1. Composition of TMR fed to all cows
the in vitro growth rate of bacteria in tears (Moraxella
bovis) or milk (Staphylococcus aureus, Escherichia coli, Item
Streptococcus uberis) collected from cows fed no kelp (d Ingredient (% of DM)
0) or kelp (d 30). We hypothesize that the tear iodine Alfalfa hay 12.73
concentration is affected by alimentary iodine uptake Grass hay 2.73
and is positively associated with serum and milk io- Corn silage 33.64
Corn gluten feed 6.36
dine concentration. Furthermore, we hypothesize that Corn grain, ground 10.91
an increased iodine concentration would decrease the Cottonseed, fuzzy (with linters) 5.00
growth rate of Moraxella bovis in tears and that of Molasses, liquid 3.63
Protein mix1 23.64
Staph. aureus, E. coli, and Klebsiella in milk compared Energy Booster2 1.36
with the original iodine concentrations in tears and Component
milk, respectively. DM (%) 59.30
CP (%) 16.50
To address objectives 1 and 2, based on the results NEM (Mcal/kg) 0.81
of Schöne et al. (2009), we expected a change in the NEG (Mcal/kg) 0.52
serum iodine concentration from 66 to 131 μg/L (SD ADF (%) 24.20
NDF (%) 33.70
~20) over the 30-d trial. Assuming 80% power and 95% Ca (%) 0.66
confidence, at least 2 cows would be needed to show P (%) 0.40
this difference in serum iodine concentration (objective 1
Protein mix included fine rolled corn (34.91%), canola meal (14.07%),
2). Therefore, 3 mid to late lactation Holstein Friesian soybean meal, 47% (12.80), SoyPass (11.31%; LignoTech, Rothschild,
WI), dry distillers grain (10.69%), blood meal (4.28%), sodium bi-
cows of the University of Minnesota’s Saint Paul cam- carbonate (3.90%), calcium carbonate (3.68%), Ultramet (1.90%;
pus dairy were enrolled per treatment to account for Vita Plus Corp., Madison, WI, including liquid MetaSmart, Adisseo,
potential losses during the study and for potentially Alpharetta, GA), potassium carbonate (1.08%), white salt (0.92%),
magnesium oxide (0.43%), and Rumensin (0.03%; Elanco Animal
lower iodine concentrations in tears. The cows were Health, Greenfield, IN) on a DM basis.
healthy and had not received kelp or other additional 2
Energy Booster 100 (Milk Specialties, Eden Prairie, MN) is hydro-
iodine supplementation previously. The Holstein Frie- genated fat.

Journal of Dairy Science Vol. 99 No. 10, 2016

8474 SORGE ET AL.

Furthermore, on d 0 and 30, duplicate aseptic com- vs. control) and initial (d 0) tear, serum, or milk io-
posite milk samples were also collected. Briefly, all teat dine concentration as fixed effects (PROC MIXED),
ends were disinfected with alcohol swabs. After dis- respectively. A paired t-test (PROC TTEST) was used
carding a squirt of milk, approximately 2 squirts were to assess the change in liver mineral, serum, milk, and
collected from all 4 teats (~50 mL total) in duplicate. tear iodine as well as thyroid hormone concentrations
In addition to the milk sample, blood samples (10-mL of cows between d 0 and 30 to account for the depen-
EDTA Vacutainer, BD) and a liver biopsy (Carriquiry dency of the data.
et al., 2009) were collected for the analysis of the thy- At the start of the study, cows of the control and
roid hormone profile [total thyroxine (T4), total tri- kelp-fed group weighed 631 ± 23 kg (mean ± SEM) and
iodothyronine (T3), free T4, free T3] and assessment 690 ± 43 kg, respectively (P = 0.31). The unadjusted
of the trace mineral status of the cows, respectively. daily DMI was 26.6 ± 0.88 and 28.8 ± 0.39 kg/d and
All samples were immediately placed on ice, processed the mean dietary iodine intake was 99.4 ± 1.91 mg
within 1 h of sampling, and frozen at −20°C before and 62.5 ± 0.85 mg/d by kelp-fed and control cows,
being sent to the Diagnostic Center for Population and respectively (P < 0.01). No difference was found be-
Animal Health of the Michigan State University for tween the daily weigh back (i.e., left over feed) between
analysis. All samples, except the liver samples, were kelp-fed (4.6% ± 4.6%) and control cows (5.5 ± 5.1%,
analyzed for iodine. Furthermore, the laboratory used P = 0.10).
T4 Monoclonal, Free T4, and Free T3 Solid phase Com- An unexpected observation was that already the
ponent System Radioimmunoassays (MP Biomedical baseline serum iodine concentration was above the ref-
Diagnostics Division, Orangeburg, NY) that were incu- erence range of 50 to 120 ng/mL (minimum: 231 ng/
bated at 37°C for 2, 1.5, and 2.5 h, respectively. Total mL) and was in the range observed for cows with hyper-
T3 was quantified with an in-house charcoal separation plastic goiter (Ong et al., 2014). The TMR contained
RIA based on Refsal et al. (1984). The Institutional inexplicably high iodine concentrations that were well
Animal Care and Use Committee of the University of above NRC (2001) suggestions of <0.6 mg/kg (Table
Minnesota approved all animal procedures before study 2), although none of the feed components included ad-
initiation. ditional iodine. However, as expected, the serum iodine
Objective 3 was addressed by using Kirby Bauer concentrations were correlated with tear (r = 0.58, P <
tests (Papich, 2013). Briefly, 50-μL aliquots of tears 0.01) as well as milk iodine levels (r = 0.54, P = 0.06,
and milk from all 3 cows fed kelp from d 0 and 30 were tendency) and increased after kelp supplementation
placed onto sterile discs that were applied to Mueller when accounting for the baseline (d 0) serum iodine
Hinton blood agar plates inoculated with Moraxella concentrations (Table 3). However, even when using all
bovis (ATCC 10900) and field isolates of Strep. uberis, available samples, tear and milk iodine concentrations
as well as Mueller Hinton plates inoculated with E. coli were not correlated (r = 0.07, P = 0.81). Furthermore,
and Staph. aureus from the Udder Health Laboratory of whereas the iodine concentration in milk (P = 0.38)
the University of Minnesota. In addition, disks soaked and tears (P = 0.17) increased only numerically over
with 50 μL of 1% iodine, 7.5% iodine, and sterile water time within groups, the milk iodine concentration on
were also placed on the plates as positive and nega- d 30 was slightly higher in the kelp-fed than control
tive controls. The iodine concentrations were selected group (P = 0.05). The observed lack of a statistically
to represent common iodine concentrations in teat dip significant differences over time within groups could be
(1%, Dinsmore and Hirst, 2002) as well as iodine con- a result of the lack of power due to the unexpectedly
centrations for killing bacteria (Salvi et al., 2006). The high baseline iodine values, which decreased the ex-
plates were incubated at 37°C with CO2 and visually pected difference between treatments. In addition, the
assessed for zones of inhibition at 24 and 48 h. tear production (total volume was not measured) may
The data were analyzed in SAS 9.4 (SAS Institute have differed between cows and days and may have
Inc., Cary, NC). The observations were reported as affected the results despite the standardization of the
mean ± standard error of the mean by group. The tear collection.
association between serum, milk, and tear iodine con- Although kelp is primarily used as an iodine supple-
centrations was assessed with Spearman correlations. ment, it is also used as a supplement for other minerals
The serum, milk, and iodine concentrations between (Sorge et al., 2016). However, liver mineral concentra-
the kelp-fed and control groups were initially compared tions did not change in either group over time (Table 3,
with a Student t-test, including Satterthwaite correc- P > 0.25). The changes in cobalt and zinc are biologi-
tion for unequal variances. Furthermore, least squares cally negligible. Overall, total T4 (40.0 ± 1.0 to 45.7 ±
means were calculated for tear, serum, and milk iodine 2.8 nmol/L), total T3 (1.8 ± 0.1 to 2.1 ± 0.1 nmol/L),
concentrations at d 30 while accounting for group (kelp free T4 (10.3 ± 0.3 to 12.7 ± 0.3 pmol/L), and free T3
Journal of Dairy Science Vol. 99 No. 10, 2016
 SHORT COMMUNICATION: TEAR IODINE CONCENTRATIONS 8475
Table 2. Mineral composition of Ascophyllum nodosum and the TMR generally within the normal range for cattle (Kafi et
on a DM basis
al., 2012), the free T3 was above the reference range
Item A. nodosum TMR (2.0–3.0 pmol/L) already at the first sampling and may
Iodine (μg/g) 743.65 2.17
be particularly influenced by the nutritional iodine
Minerals (mg/kg) intake (Ong et al., 2014). Whether this had clinical
Sodium 42,340 5,656 implications is not clear because we did not specifically
Sulfur 28,169 2,877 assess the thyroid glands.
Potassium 28,007 13,208
Calcium 13,137 7,741 Although a previous study had shown some antibac-
Magnesium 8,255 3,708 terial activities of Ascophyllum nodosum extracts in vi-
Phosphorus 1,637 4,007 tro (Vacca and Walsh, 1954), milk and tears from study
Iron 204 395
Boron 108.9 10.6 cows did not prevent the in vitro growth of any of the
Aluminum 75.6 257 tested bacteria, including Moraxella bovis, regardless of
Arsenic 28.3 <2.5 their iodine levels or which group they were from. In
Manganese 15.6 85.8
Barium 4.7 7 contrast, 1 and 7.5% iodine positive controls did show
Copper 1.7 18.6 inhibition of bacterial growth. Therefore, the hypoth-
Cobalt 1.45 1.3 esis that the iodine concentration of tears has a direct
Cadmium 0.9 <0.3
Thallium <12.5 <12.5 effect on the growth of, for example, Moraxella bovis
Selenium <10.0 <10.0 could not be confirmed, but it remains unclear how or
Mercury <10.0 <10.0 if the previously demonstrated antibacterial properties
Molybdenum <1.0 <1.0
Lead <2.5 <2.5 (Vacca and Walsh, 1954) translate to kelp fed to and
Chromium <1.0 <1.0 digested by ruminants. Siddiqui (1993) speculated that
Antimony <5.0 <5.0 inorganic iodine by itself may decrease bacterial growth
or could improve immune function. Indeed, studies have
shown that iodine supplementation increased the iodide
(3.7 ± 0.2 to 5.0 ± 0.6 pmol/L) serum concentrations concentration in the upper respiratory tract (Fischer
did not change over the course of the experiment in the et al., 2011; Derscheid et al., 2014) and decreased the
kelp-fed group (P > 0.05). This is similar to the obser- severity of respiratory syncytial virus disease in lambs
vations by Antaya et al. (2015) who also did not find (Derscheid et al., 2014) by improving the immune func-
changes in the thyroid hormones after supplementation tion (Fischer et al., 2011; Derscheid et al., 2014). Simi-
with kelp. However, although the concentrations were larly, supplementation with iodine was associated with

Table 3. Serum, milk, and tear iodine and liver mineral concentrations (mean ± SEM) of kelp- and control-fed cows at the beginning (d 0) and
end of the experiment (d 30)

Kelp Control

Item d0 d 30 d0 d 30
Cows (no.) 3 3   3 3
Iodine (ng/mL)          
Serum1 265 ± 38b 429 ± 5a   311 ± 40b 305 ± 5b
Milk1 531 ± 31ab 660 ± 83a   425 ± 34b 517 ± 83b
Tears1 1,122 ± 360 1,225 ± 104   958 ± 25 960 ± 104
Liver minerals (mg/kg)          
Arsenic 0.03 ± 0 0.02 ± 0.01   0.03 ± 0 0.03 ± 0
Cadmium 0.08 ± 0.01 0.07 ± 0.01   0.10 ± 0.02 0.10 ± 0.02
Lead 0.17 ± 0.09 0.31 ± 0.24   0.10 ± 0.05 0.10 ± 0.02
Mercury 0.13 ± 0 0.13 ± 0   0.13 ± 0 0.13 ± 0
Thallium 0.03 ± 0 0.03 ± 0   0.03 ± 0 0.03 ± 0
Cobalt 0.42 ± 0.01a 0.38 ± 0.01b   0.35 ± 0.01 0.35 ± 0.05
Iron 266a ± 5.36 307 ± 37.60   392b ± 78.9 395 ± 39.73
Manganese 14.07 ± 1.47 11.88 ± 0.43   10.54 ± 0.44 11.65 ± 0.79
Molybdenum 4.49 ± 0.26 4.17 ± 0.04   3.54 ± 0.18 4.15 ± 0.26
Selenium 4.15 ± 0.66 3.86 ± 0.68   3.94 ± 0.61 2.63 ± 0.18
Zinc 123a ± 15.41 105 ± 7.64ab   114b ± 2.19 111b ± 4.91
a,b
Different superscripts in a row indicated statistical differences based on a Student-t-test between groups on d 0 and 30 and a paired t-test
within kelp-fed and control cows over time.
1
The averages at d 30 are LSM based on a linear regression including group and iodine concentration (serum, milk, tears, respectively) at d 0
as fixed effects.

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8476 SORGE ET AL.

a decreased incidence of foot rot, a bacterial disease, 2014. Increased concentration of iodide in airway secretions is as-
sociated with reduced respiratory syncytial virus disease severity.
in feedlot cattle (Berg et al., 1984; Maas et al., 1984). Am. J. Respir. Cell Mol. Biol. 50:389–397.
Therefore, one could speculate that iodine from kelp Dinsmore, P., and H. Hirst. 2002. What about this new teat dip?
could potentially be supportive of the immune system Accessed Feb. 4, 2016. https://www.cvmbs.colostate.edu/ilm/
proinfo/cdn/2002/Teat%20DipMay02.pdf.
against infectious bacteria. However, in our study the Fischer, A. J., N. J. Lennemann, S. Krishnamurthy, P. Pocza, L. Du-
tears had been centrifuged and frozen and so a poten- rairaj, J. L. Launspach, B. A. Rhein, C. Wohlford-Lenane, D. Lo-
tial effect of increased iodine levels through the local rentzen, and B. Banfi. 2011. Enhancement of respiratory mucosal
antiviral defenses by the oxidation of iodide. Am. J. Respir. Cell
immune system could not be assessed. Mol. Biol. 45:874–881.
In summary, serum iodine concentration was corre- Kafi, M., A. Tamadon, M. Saeb, A. Mirzaei, and M. Ansari-Lari. 2012.
lated with the iodine concentration in milk and tears. Relationships between thyroid hormones and serum energy me-
tabolites with different patterns of postpartum luteal activity in
However, the feeding of kelp only increased the iodine high producing dairy cows. Animal 6:1253–1260.
levels in serum of cows in this study and the iodine con- Maas, J., L. E. Davis, C. Hempstead, J. N. Berg, and K. A. Hoff-
centrations in milk and tears changed only numerically man. 1984. Efficacy of ethylenediamine dihydriodide in the pre-
vention of naturally occurring foot rot in cattle. Am. J. Vet. Res.
and were not associated with an inhibition of bacterial 45:2347–2350.
growth in vitro. Therefore, a prevention of infectious NRC. 2001. Nutrient Requirements of Dairy Cattle. 7th ed. National
bovine keratoconjunctivitis would probably not be Academy of Sciences, Washington, DC.
Olree, R., and P. Dettloff. 2010. Kelp and dairy cattle pilot study. Ac-
based solely on increased iodine concentrations in tears. cessed Apr. 30, 2014. http://grassworks.org/?300604/conf.Orlee.
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Ong, C. B., T. H. Herdt, and S. D. Fitzgerald. 2014. Hyperplastic
ACKNOWLEDGMENTS goiter in two adult dairy cows. J. Vet. Diagn. Invest. 26:810–814.
Papich, M. D. 2013. VET01–A4: Performance Standards for Antimi-
We thank Nathanial McDonald, Wyatt Smith, and crobial Disk and Dilution Susceptibility Tests for Bacteria Isolated
Angel M. Rosales Gallardo (Dept. of Animal Science, From Animals; Approved Standard, 4th ed. Clinical and Labora-
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University of Minnesota, St. Paul) for their help during Refsal, K. R., R. F. Nachreiner, and C. R. Anderson. 1984. Relation-
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thyroxine and triiodothyronine in Holstein cows. Domest. Anim.
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