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(Investigative Ophthalmology and Visual Science. 2003;44:2722-2729.)
© 2003 by The Association for Research in Vision and Ophthalmology, Inc.
DOI:  10.1167/iovs.02-1283
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Light-Absorbing Properties and Osmolarity of Indocyanine-Green Depending on Concentration and Solvent Medium

Christos Haritoglou,1,2 Arnd Gandorfer,1,2 Markus Schaumberger,1 Ramin Tadayoni,3 Achim Gandorfer,4 and Anselm Kampik1

1From the Department of Ophthalmology, Ludwig-Maximilians-University, Munich, Germany; the 3Department of Ophthalmology, Hôpital Lariboisière, Assistance Publique-Hôpitaux de Paris, Université Paris, Paris, France; and the 4Institute of Astronomy, Swiss Federal Institute of Technology, Zürich, Switzerland.


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
PURPOSE. To evaluate the absorption spectrum and osmolarity of three currently used indocyanine green (ICG) products at different concentrations and with different solvent media.

METHODS. The absorption spectrum and osmolarity of three different ICG products (Pulsion, Munich, Germany; Akorn, Buffalo Grove, IL; and Laboratoires SERB, Paris, France) were analyzed. Each ICG was further diluted with balanced salt solution or glucose 5%. Four different concentrations were evaluated: 0.005%, 0.0025%, 0.001%, and 0.00025%. ICG (Pulsion) diluted in viscoelastic material (Healon; Pharmacia, Stockholm, Sweden) was analyzed at a concentration of 0.0025%. The following parameters were measured: absorption spectrum between 400 and 1000 nm, osmolarity, and the emission spectrum of the light source of a commonly used vitrectomy machine (Megatron; Geuder, Heidelberg, Germany).

RESULTS. Independent from the manufacturer, concentrations of 0.005%, 0.0025%, and 0.001% ICG diluted in balanced salt solutions (BSS and BSS Plus; Alcon Pharmaceuticals, Fort Worth, TX) and glucose 5% showed two maxima, one at approximately 700 nm and a second one at 780 nm. There was an increase from zero to maximum absorption between 600 and 700 nm and a return to zero between 800 and 900 nm. The absorption band of ICG diluted in the viscoelastic material was similar to the saline solution (BSS or BSS Plus)-diluted ICG. At lower concentrations of 0.001% or 0.00025%, the peak at 700 nm decreased, forming a shoulder in the curve, whereas the peak at 780 nm remained stable. Osmolarity was in the range of 302 to 313 mOsM for BSS Plus-diluted ICG. When glucose 5% was used for ICG dilution, absorption between 600 and 700 nm decreased, and osmolarity was lower (between 292 and 298 mOsM). The light source emission was between 380 and 760 nm.

CONCLUSIONS. Dilution of ICG using the balanced salt solutions BSS or BSS Plus resulted in a steep increase of absorption starting at 600 nm. In clinical practice, there is an overlap between the absorption band of ICG and the emission curve of the light source, resulting in a possible photosensitizing effect, especially at higher ICG concentrations. This effect becomes less likely with decreasing ICG concentrations or when glucose 5% is used as a solvent medium.

In ophthalmology and other medical fields, indocyanine green (ICG) is commonly used as a dye for angiography and has a long history of safety. In addition, studies have demonstrated that ICG stains the internal limiting membrane (ILM),1 2 3 resulting in better visibility and easier removal of this delicate structure. As a consequence, use of ICG has become popular, especially in macular hole surgery, where ILM removal seems to be beneficial for functional and anatomic success.4 5 6 Although encouraged by these reports, we soon realized that functional outcome after ICG-assisted surgery is less favorable than results without ICG.7 8 9 Experimental and clinical data suggest possible adverse effects on the retina and functional outcome.10 11 12 The underlying pathomechanism is still not understood.

So far, there is no standardized ICG product with proven safety for intraocular application. At present, different ICG products and solvent media such as the balanced salt solutions BSS3 and BSS Plus8 (both from Alcon, Inc., Fort Worth, TX) or viscoelastic material2 (Healon; Pharmacia, Stockholm, Sweden), as well as various concentrations of ICG solutions, are applied during vitreomacular surgery.

This study was performed to elucidate possible variations between different ICG products in absorption spectrum and osmolarity at different concentrations when used with different solvent media, with the intent of creating a standardized ICG solution with no potential toxicity.


   Methods
Top
 Abstract
 Methods
Results
 Discussion
 References
 
Three different ICG products were analyzed and termed ICG-Pulsion (Pulsion, Munich, Germany), ICG-Akorn (Akorn, Buffalo Grove, IL), and Infracyanine (Laboratoires SERB, Paris, France). The ICG powder was first dissolved as suggested by the manufacturer. Each solution was then further diluted with balanced salt solution (BSS or BSS Plus; Alcon, Inc.) or glucose 5% (Baxter, Unterschleissheim, Germany). Solutions of a concentration of 0.005%, 0.0025%, 0.001%, and 0.00025% were prepared. The measurement of an initial ICG concentration of 0.005% was chosen to imitate our clinical setting,8 in which approximately 0.2 mL of 0.05% ICG was injected into the fluid-filled globe with an assumed volume of 4 mL, resulting in ICG concentrations of 0.0025% or higher. The intraocular ICG concentration decreases when the dye is washed out during surgery. ICG from one manufacturer (Pulsion) was additionally diluted in viscoelastic material (10 mg/mL Healon; Pharmacia) and measured at a concentration of 0.0025%.

The absorption spectrum of each sample was measured on a spectrophotometer (model U2000; Hitachi, Tokyo, Japan) between 400 and 1000 nm, with a scan rate of 200 nm per minute. To evaluate further the apparent differences of the absorption spectrum at higher concentrations (0.005% or 0.0025%), these concentrations were measured again with BSS, BSS Plus, glucose 5%, and Healon as a reference to obtain absolute values. Osmolarity was measured on a osmometer (model 2400; Fiske Associates, Norwood, MA).

All measurements were repeated twice. After preparation, the samples were analyzed within a duration of less than 30 minutes. The spectral irradiance of the cold light source (Megatron; Geuder, Heidelberg, Germany) was used from an earlier investigation, as described previously.12

To be able to analyze and compare the different absorption spectra, we scanned the printouts of the spectrophotometer (resolution 300 dpi) and digitized them on computer (UN-SCAN-IT 5.0; Silk Scientific Corp., Orem, UT). Each curve was digitized two times, by using the options "follow top surface of line" and "follow bottom surface of line." The resultant 18 data sets consisted of approximately 1550 wavelength-absorption data pairs and were each imported into a statistical analysis program (SPSS for Windows 10.0; SPSS Science, Chicago, IL). For further analysis, each data set was reduced to one absorption value per nanometer wavelength, calculated as the mean of all absorption values within intervals of a 1-nanometer width (e.g. 500.0000–500.9999 nm). The resultant data of the "follow top" and "follow bottom" digitizing runs were averaged. Further, these 600 spectral absorption values at wavelengths from 401 to 1000 nm are referred to by the term absorption curve of the ICG solution, if not stated otherwise. The relative spectral intensity data of the light source was determined accordingly.

To understand the relevance of the differences in the spectral absorption coefficients and absorption curves more clearly, weighted absorption coefficients were diagrammed. These were calculated by multiplying the absorption coefficient for each wavelength by the corresponding relative intensity of the cold light source. By this means absorption coefficients at wavelengths of high relative intensity (e.g., approximately 550 nm) are given more emphasis than the ones at wavelengths of 700 nm and above.


   Results
Top
 Abstract
 Methods
 Results
Discussion
 References
 
Absorption Properties of ICG
At concentrations of 0.005%, 0.0025%, and 0.001%, the absorption spectrum of ICG diluted in BSS, BSS Plus, and glucose 5% showed a double-peaked curve with two maxima, one at approximately 700 nm and a second one between 780 to 800 nm. Concerning the first peak, there was an increase from zero to maximum absorption between 600 and 700 nm. A return to zero occurred between 800 and 900 nm. The maximum of the absorption coefficient varied, depending on the solvent medium. At lower concentrations of 0.001% or 0.00025% the peak at 700 nm decreased and converted into a shoulder. In contrast, the peak at 780 nm remained stable with a decreasing absorption coefficient, even at lower concentrations. At concentrations of 0.005% to 0.001%, we observed a more concave curve between 600 and 700 nm, suggesting less absorption when using glucose 5% for ICG dilution (Fig. 1) .



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  		FIGURE 1. Absorption spectra of ICG-Pulsion diluted in BSS Plus (left column), BSS (middle column), and glucose 5% (right column). Spectra of concentrations of 0.005% (top row), 0.001% (middle row), and 0.00025% (bottom row) are shown. At concentrations of 0.005% and 0.001%, the absorption spectrum of ICG showed a double-peaked curve with two maxima at 700 and 780 nm, independent of the solvent medium. The maximum of the absorption coefficient varied depending on the solvent medium. At lower concentrations of 0.00025% the peak at 700 nm converted into a shoulder, whereas the peak at 780 nm remained stable, with a decreasing absorption coefficient at lower concentrations. Note the decrease of absorption between 600 and 700 nm of glucose 5%-diluted ICG. The spectra were similar for the other two ICG products.

 
The comparison of different ICG products revealed the following: When glucose 5% was used as a solvent medium, the absorption between 600 and 700 nm was decreased, compared with the absorption with BSS or BSS Plus, as described earlier, independent from the ICG product. However, the maximum of the absorption coefficient was variable. As in BSS- or BSS Plus-diluted ICG, the peak at 780 nm was stable when glucose 5% was used for dilution (Fig. 2) .



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  		FIGURE 2. Absorption spectra of ICG-Pulsion (top), ICG-Akorn (middle), and Infracyanine (bottom) at a concentration of 0.0025% using BSS, BSS Plus, and glucose 5% as a solvent medium. Whereas the spectra of BSS and BSS Plus are very similar, a decrease of absorption occurred between 600 and 700 nm when glucose 5% was used for dilution. No differences between the ICG products, except a variable maximum of the absorption coefficient were found. As was the case with BSS- or BSS Plus-diluted ICG, the peak at 780 nm was stable when glucose 5% was used for dilution.

 
In the weighted curves, the differences between the ICG solutions became more apparent: BSS- and BSS Plus-diluted ICG showed maxima at lower wavelengths of approximately 630 nm in contrast to glucose 5%-diluted ICG, with a maximum at approximately 690 nm; in addition, the maximum absorption coefficient was lower when glucose 5% was used for dilution of ICG-Pulsion and ICG-Akorn (Fig. 3) .



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  		FIGURE 3. Weighted curves of ICG-Pulsion (top), ICG-Akorn (middle), and Infracyanine (bottom) at a concentration of 0.0025%, with BSS, BSS Plus, and glucose 5% used for dilution. The shift of the absorption spectra comparing the ICG solutions became more apparent: BSS- and BSS Plus-diluted ICG showed maxima at lower wavelengths of approximately 630 nm in contrast to glucose 5%-diluted ICG, with a maximum at approximately 690 nm; in addition, the maximum absorption coefficient was lower when glucose 5% was used for dilution of ICG-Pulsion and ICG-Akorn.

 
For Healon-diluted ICG (Pulsion) with a concentration of 0.0025% a very similar curve compared to BSS- or BSS Plus-diluted ICG was obtained (Fig. 4) .



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  		FIGURE 4. A 0.0025% ICG-Healon mixture showed absorption properties similar to those of BSS- or BSS Plus-diluted ICG. As with BSS- and BSS Plus-diluted ICG, the maximum of the weighted curve appeared at approximately 630 nm.

 
Emission Spectrum of the Light Source
The vitrectomy machine contains a new halogen bulb (24 V, 150 W). The spectral irradiance of the cold light source of our standard vitrectomy machine (Megatron; Geuder) was measured at the end of the fiberoptic, as described recently.12 The light source emission was between 380 and 760 nm. No irradiance was measured below 380 and beyond 760 nm. As described previously,12 28% of the total irradiance emission was beyond 600 nm (Fig. 5) .



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  		FIGURE 5. The cold light source of the vitrectomy instrument emitted between 380 and 760 nm. No irradiance was measured below 380 nm or beyond 760 nm. Of the total irradiance, 28% was emitted beyond 600 nm.

 
Osmolarity
For BSS- or BSS Plus-diluted ICG, the osmolarity was in the range of 302 to 313 mOsM. The osmolarity of BSS or BSS Plus alone was measured to be 307 mOsM and 314 mOsM, respectively. The osmolarity of glucose 5% diluted ICG was lower and ranged between 292 and 298 mOsM. The osmolarity of glucose 5% alone was 298 mOsM. The osmolarity of Healon was measured to be 275 and 272 mOsM for a 0.0025% ICG-Healon mixture. The complete data are presented in Table 1 .


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  		TABLE 1. Osmolarity of ICG Pulsion, ICG Akorn and Infracyanine

 

   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
References
 
Shortly after the introduction of ICG in macular surgery, our surgical approach4 9 was modified by the intraoperative application of commercially available ICG (Pulsion), which was diluted with BSS Plus (Alcon, Inc.), as reported previously.7 8 BSS Plus was also used as an irrigation solution during surgery.

To our surprise, functional results after ICG-assisted vitrectomy in macular hole surgery did not compare favorably with those in a prospective study incorporating a large number of patients after ILM peeling without ICG staining.9 There was not only less benefit in terms of visual acuity, but also an increased number of visual field defects.8 The closure rate was not affected. Histologic analysis of tissue removed during surgery showed obvious differences between the stained and unstained ILM.7 8 However, we were convinced that morphologic findings alone did not account for this unexpected finding.

As a consequence, additional factors were systematically analyzed. First of all, the osmolarity of our ICG solution was evaluated. The measured osmolarity of 275 mOsM8 corresponded well to those reported by other groups2 3 13 14 that did not report adverse effects after the use of ICG and differed only slightly from the osmolarity of BSS Plus, which is 305 mOsM.15

In 1976 Landsman et al.16 published a report on the spectral absorption properties of ICG. Besides other information on stability and spectral stabilization of ICG, they showed that the absorption spectrum of ICG depends on the nature of the solvent medium and on the concentration. Increasing ICG concentration results in progressive formation of aggregate. This report encouraged us to investigate further the absorption properties of ICG.

Up to now, there has been no protocol for ICG preparation for vitreomacular surgery, resulting in a standardized ICG solution with a defined concentration. In the literature, the concentration varies from 0.05%,8 to 0.06%,2 to 0.5%.3 Of note, ICG is further diluted when injected into the fluid-filled globe, with an assumed volume of 4 mL. For example, the injection of 0.2 mL of 0.05% ICG results in an intraocular ICG concentration of 0.0025% or higher. The intraocular ICG concentration then further decreases when ICG is washed out thereafter, during surgery. To imitate the intraoperative situation of decreasing intraocular ICG concentrations and possible subsequent changes of the absorption spectrum, we analyzed the light-absorbing properties of different ICG solutions with a concentration of 0.005% or less. ICG diluted in Healon was measured only at a concentration of approximately 0.0025%, because it was difficult to dilute ICG with viscoelastic material and obtain solutions of decreasing and reliable concentrations. However, the absorption spectrum of 0.0025% Healon-diluted ICG was similar to BSS- or BSS Plus-diluted ICG (Fig. 4) .

As reported herein, there were differences in absorption, depending on the solvent medium, regardless of the ICG product itself. As our cold light source emitted between 380 and 760 nm, there was a theoretical overlap of the emission and absorption spectrum between 400 and 760 nm, with significant absorption between 600 and 760 nm, especially when BSS or BSS Plus was used for dilution. The differences between BSS/BSS Plus- and glucose 5%-diluted ICG decreased when the concentration was lowered. The possible interference with the emission spectrum of the intraocular illumination source might induce a photosensitizing effect on the retina. Their term "photodynamic" may not be appropriate in the context of our experimental setting, because a photodynamic effect involves the generation of reactive oxygen species which was not demonstrated here. However, our experiment does indicate a possible photosensitizing effect. The use of ICG as an ideal photosensitizer has been described previously, not only in ophthalmology, but also in other medical fields.16 17 18 Recently, an experimental surgical approach in human donor eyes revealed inner retinal damage after the use of ICG and illumination, using wavelengths between 600 and 760 nm.12 The amount of absorption may well be influenced by the amplitude of the absorption coefficient. As shown in Figures 1 and 2 , higher absorption coefficients were measured when glucose 5% was used as a solvent medium. However, there was a shift of the absorption band of glucose 5%-diluted ICG toward higher wavelengths, where far less emission was measured (Fig. 5) . Therefore, the risk of higher absorption was minimized, despite higher absorption coefficients (as shown in Fig. 3 ).

Not included in this investigation, the following factors may also have an influence and should be considered: (1) the actual concentration of ICG bound to the ILM at the vitreoretinal interface; and (2) the role of air versus BSS Plus filling the vitreous cavity during the staining process.

In summary, this study provides further evidence that the dilution of ICG in different solvent media results in a shift of the absorption band of ICG toward wavelengths commonly used during surgery. It is theoretically possible to induce a photosensitizing effect on the retinal surface when using ICG in macular surgery. This effect seems to be lower when glucose 5% is used for ICG dilution. To obtain an ICG solution that is safe for intraocular application in vitreomacular surgery, the concentration and absorption characteristics of the dye and its dilution must be considered.


   Acknowledgements
 
The authors thank Michael Vogeser, Björn Hennel, and Emil Egeler for excellent technical support.


   Footnotes
 
2 Contributed equally to the work and therefore should be considered equivalent authors. Back

Submitted for publication December 15, 2002; revised January 24, 2003; accepted February 3, 2003.

Disclosure: C. Haritoglou, None; Ar. Gandorfer, None; M. Schaumberger, None; R. Tadayoni, None; Ac. Gandorfer, None; A. Kampik, None

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Corresponding author: Christos Haritoglou, Department of Ophthalmology, Ludwig-Maximilians-University, Mathildenstr. 8, 80336 Munich, Germany; christos.haritoglou{at}ak-i.med.uni-muenchen.de.


   References
Top
 Abstract
 Methods
 Results
 Discussion
 References
 

  1. Gandorfer, A, Messmer, EM, Ulbig, MW, Kampik, A. (2001) Indocyanine green selectively stains the internal limiting membrane Am J Ophthalmol 131,387-388[CrossRef][Medline][Order article via Infotrieve]
  2. Kadonosono, K, Itoh, N, Uchio, E, Nakamura, S, Ohno, S. (2000) Staining of the internal limiting membrane in macular hole surgery Arch Ophthalmol 118,1116-1118[Abstract/Free Full Text]
  3. Burk, SE, Da Mata, AP, Snyder, ME, Rosa, RH, Foster, RE. (2000) Indocyanine green-assisted peeling of the retinal internal limiting membrane Ophthalmology 107,2010-2014[CrossRef][Medline][Order article via Infotrieve]
  4. Haritoglou, C, Gass, CA, Schaumberger, M, Ehrt, O, Gandorfer, A, Kampik, A. (2001) Macular changes after peeling of the internal limiting membrane in macular hole surgery Am J Ophthalmol 132,363-369[CrossRef][Medline][Order article via Infotrieve]
  5. Brooks, HL, Jr (2000) Macular hole surgery with and without internal limiting membrane peeling Ophthalmology 107,1939-1949[CrossRef][Medline][Order article via Infotrieve]
  6. Liesenhoff, O, Messmer, EM, Pulur, A, Kampik, A. (1996) Treatment of full thickness idiopathic macular holes Ophthalmologe 93,655-659[CrossRef][Medline][Order article via Infotrieve]
  7. Gandorfer, A, Haritoglou, C, Gass, CA, Ulbig, MW, Kampik, A. (2001) ICG-assisted peeling of the internal limiting membrane may cause retinal damage Am J Ophthalmol 132,431-433[CrossRef][Medline][Order article via Infotrieve]
  8. Haritoglou, C, Gandorfer, A, Gass, CA, Ulbig, MW, Kampik, A. (2002) Indocyanine green-assisted peeling of the internal limiting membrane in macular hole surgery affects visual outcome: a clinicopathologic correlation Am J Ophthalmol 143,836-841
  9. Haritoglou, C, Gass, CA, Schaumberger, M, Gandorfer, A, Ulbig, MW, Kampik, A. (2002) Long term follow-up after macular hole surgery with internal limiting membrane peeling Am J Ophthalmol 134,661-666[CrossRef][Medline][Order article via Infotrieve]
  10. Sippy, BD, Engelbrecht, NE, Hubbard, GB, et al (2001) Indocyanine green effect on cultured human retinal pigment epithelial cells: implication for macular hole surgery Am J Ophthalmol 132,433-435[CrossRef][Medline][Order article via Infotrieve]
  11. Enaida, H, Sakamoto, T, Hisatomi, T, Goto, Y, Ishibashi, T. (2002) Morphological and functional damage of the retina caused by intravitreous indocyanine green in rat eyes Graefes Arch Clin Exp Ophthalmol 240,209-213[CrossRef][Medline][Order article via Infotrieve]
  12. Gandorfer, A, Haritoglou, C, Gandorfer, A, Kampik, A. (2003) Retinal damage from ICG in experimental macular surgery Invest Ophthalmol Vis Sci 44,316-323[Abstract/Free Full Text]
  13. Da Mata, AP, Burk, SE, Riemann, CD, et al (2001) Indocyanine green-assisted peeling of the retinal internal limiting membrane during vitrectomy surgery for macular hole repair Ophthalmology 108,1187-1192[CrossRef][Medline][Order article via Infotrieve]
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A. Gandorfer, M. Rohleder, C. Sethi, D. Eckle, U. Welge-Lussen, A. Kampik, P. Luthert, and D. Charteris
Posterior Vitreous Detachment Induced by Microplasmin
Invest. Ophthalmol. Vis. Sci., February 1, 2004; 45(2): 641 - 647.
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