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Public Information Notice (PIN) No. 03/112
September 5, 2003
International Monetary Fund
700 19th Street, NW
Washington, D.C. 20431 USA

IMF Concludes 2003 Article IV Consultation with Japan

On August 20, 2003, the Executive Board of the International Monetary Fund (IMF) concluded the Article IV consultation with Japan.1

Japan experienced a cyclical recovery in 2002, which included a strong pickup on activity in the second quarter followed by a gradual slowdown during the rest of the year. For 2002 as a whole, real GDP grew by only 0.2 percent, owing to the low base for the recovery that resulted from the sharp fall in output during the previous year.

During the first half of 2003, GDP growth was stronger than initially expected, although deflation continued. According to the first preliminary estimate, real GDP rose significantly in the second quarter, compared with consensus forecasts of little growth. Consumption, business fixed investment, and net exports were stronger than implied by monthly indicators. Notwithstanding the pickup in demand, the unemployment rate has remained near its record high, and the GDP deflator has continued to fall, extending the year-on-year declines that have been ongoing since 1998. The core CPI (excluding fresh food) has also decreased year on year virtually every month for about the past four years. Meanwhile, expectations of deflation remain entrenched.

Monetary policy has remained focused on maintaining financial stability, primarily by providing liquidity to ensure that banks could meet their funding needs without difficulties. Over the past 12 months the Bank of Japan (BoJ) raised the target for current account balances on several occasions, periodically injected liquidity, expanded the range of collateral eligible for operations, and removed the restriction on the maximum number of days for the use of Lombard loans, beyond which the penalty rate was applied. The BoJ has also helped banks reduce their equity risk with its program to buy banks' shareholdings for up to ¥3 trillion through September 2003. A program of outright purchases of asset-backed securities, up to ¥1 trillion through March 2006, commenced at end-July 2003.

Growth in base money has not fed into broad monetary aggregates or arrested the continuous decline in bank lending, although short-term interest rates have been kept at virtually zero. With persistent economic weaknesses and bank balance sheet problems limiting loan demand and banks' willingness to lend, bank loans continued declining by about 5 percent a year.

Fiscal policy was expansionary in FY2002, as the general government structural deficit widened by about 1 percent of GDP to 6½ percent of GDP. Unadjusted, the deficit rose to 7½ percent of GDP, mainly reflecting a fall in revenue. Continued fiscal deficits have fed rapidly growing government debt, with end-2002 gross and net debt estimated at 158 and 72 percent of GDP respectively.

In the external sector, the favorable trade performance in 2002 raised the current account surplus by about ¾ percent of GDP to 2¾ percent of GDP. Export volume rose strongly, reflecting a sharp pickup in demand from Asian partner countries (notably China) and the United States, although volume growth slowed in the second half of the year. Imports recovered along with domestic income, partly reflecting a pickup in imports from China.

Compared to June 2002, the yen is broadly unchanged against the U.S. dollar but is modestly weaker in nominal and real effective terms. In the second half of 2002, the yen/dollar rate ranged between ¥116 and ¥125 amid heightened geopolitical uncertainty and concerns about the pace and sustainability of recovery in the major economies. In the first seven months of 2003, the yen came under pressure to strengthen against the dollar, as the dollar weakened against the euro. This pressure prompted the authorities to intervene on a number of occasions over this period, in the total amount of some ¥9 trillion. In the event, for most of 2003 to date the yen/dollar rate has moved in a range of ±¥2 around ¥119. The yen has weakened against the euro, however, contributing to depreciation in real and nominal effective terms.

Long-term government bond yields hit record lows in June 2003 but subsequently rebounded. The decline in yields in the face of high and rising government debt partly reflected heavy buying of Japanese Government Bonds (JGBs) by financial institutions amid ample liquidity, weak loan demand, increased risk aversion, and banks' efforts to cut risk-weighted assets. The BoJ has also made outright purchases of JGBs, amounting to ¥1.2 trillion per month since October 2002. Starting in late June 2003, long-term yields rebounded. The rise in JGB yields, which occurred in the context of a less pronounced global pickup in long-term interest rates, may have reflected financial market considerations such as portfolio rebalancing from bonds to equities, profit-taking, and investor concerns that yields had fallen too far. Alternatively, it may have reflected a perceived improvement in economic prospects.

Stock prices have also recently recovered from long-term lows. During most of the past 12 months, stock prices have fallen amid concerns about selling pressures from banks and pension funds. In early 2003, the Nikkei index declined broadly in line with other mature markets, but from already low levels, and in April bottomed out at 21-year lows. On the heels of rallies in overseas markets, the Nikkei subsequently rebounded largely driven by foreign buying. As of mid-August 2003, the Nikkei was up about 18 percent for the year and about 7 percent higher than a year earlier. The rise in stock prices during recent months has boosted the value of equities on bank balance sheets, while the increase in interest rates has reduced the value of bond holdings; as of August it was unclear whether the net effect on bank balance sheets was positive or negative.

Financial institutions' end-FY2002 results revealed some progress in dealing with their problems, but their financial difficulties persisted. Major banks' average ratio of nonperforming loans to credit declined from 8½ percent to 7¼ percent during the fiscal year, in line with the authorities' target to halve the ratio by end-FY2004. However, major banks' losses from equity holdings together with credit costs resulted in net losses of ¥4.4 trillion. Meanwhile, life insurers faced continued pressures from their equity exposures and high guaranteed rates on existing policies.

Data on stronger second-quarter growth along with other factors has led to an improvement in the outlook. Although national accounts data are subject to substantial revisions, GDP estimates for the first half of 2003 and more optimistic projections for partner countries imply that the pickup in activity may have begun earlier than previously anticipated. Incorporating such factors, real GDP is expected to grow by 2 percent in 2003 and 1½ percent in 2004. However, while the recent increase in stock prices and the firmer external environment suggest that the risks to the outlook may have become more balanced, important downside risks are still associated with the remaining fragilities on corporate and financial sector balance sheets.

Executive Board Assessment

Directors welcomed recent signs of improvement in the economic situation and outlook, and the progress in tackling the major economic challenges facing Japan. The volume of banks' nonperforming loans has declined, and corporate profits have increased. Supportive monetary policy has helped maintain financial stability and may have also contained deflation.

Nevertheless, Directors stressed that serious and interrelated problems remain, and that a sustained and strong economic revival is not yet in prospect. Significant weaknesses still exist in the financial and corporate sectors, which, if not resolved, will continue to restrain growth. Deflation is likely to persist and continue to exacerbate corporate and financial sector fragilities. A substantial medium-term adjustment in fiscal policies is still needed to prevent public debt from rising to levels that could put upward pressure on real interest rates, with negative implications for growth and the financial system. The economy remains vulnerable to significant downside risks, notably those associated with fragilities in corporate and financial sector balance sheets.

Directors agreed that a more comprehensive and integrated policy approach is needed to revitalize the corporate and financial sectors, tackle deflation, and address fiscal imbalances. They broadly endorsed the staff's recommended strategy involving four interrelated pillars of accelerated financial and corporate sector reforms, attacking deflation more aggressively through monetary policy, and implementing a framework for medium-term fiscal consolidation. Directors acknowledged that accelerated reforms could entail short-term economic costs, but most Directors considered that these costs are outweighed by the medium-term benefits of reduced vulnerability and higher potential growth. They also stressed that the social safety net and a more proactive labor market policy could mitigate the effects of adjustment and restructuring. However, a few Directors felt that in light of the potential severity of the short-term costs, a more cautious approach would be advisable.

Directors welcomed Japan's participation in the Financial Sector Assessment Program (FSAP), although a few Directors noted that more complete information should have been made available for stress testing the exposure of the banking system. Directors also welcomed the progress made in financial sector restructuring under the Program for Financial Revival (PFR). Most Directors considered that a more comprehensive and accelerated approach to financial sector reforms, in line with the FSAP recommendations, is still needed in order to tackle decisively the problems in banks and insurance companies. In this context, recent measures to address the problem of nonperforming loans should be applied to a wider set of loans and institutions, and supervisory-mandated provisions should be recognized as a cost for tax purposes. The regulation of insurance companies, which remain vulnerable to a deterioration in financial markets, should also be enhanced.

Directors observed that some banks had recently strengthened their capitalization by raising capital in the markets, but they also noted that banks' regulatory capital relies too heavily on deferred tax assets (DTAs). Against this background, most Directors agreed with the recommendation to limit the use of DTAs as regulatory capital. Most Directors concurred that, given the lack of private interest in recapitalizing banks, public funds might have to be used selectively to recapitalize systemically important banks that fell below regulatory capital requirements, and that any transitional period of government ownership should be used to strengthen bank governance. A few Directors were concerned that this would nevertheless lead to undesirable government involvement. Directors agreed in general that reducing the involvement of government institutions in the financial sector could improve bank profitability. In the same vein, the requirement that banks that receive public funds commit to lend more to small- and medium-sized enterprises should not be imposed.

Directors observed that a durable resolution of banks' problems and the achievement of sustained growth over the medium term will require further progress in corporate sector restructuring, including small- and medium-sized enterprises, where progress has been slow. Further strengthening the banking system will be critical to speed up corporate restructuring, as banks must be able to absorb losses arising from restructuring. The Industrial Revitalization Corporation of Japan (IRCJ) could facilitate restructuring by helping to coordinate creditors, but it should not be used to keep nonviable firms afloat. Minimizing the period between the IRCJ's purchase and sale of loans, and ensuring transparency regarding its operations and progress in recovering public funds, would help to mitigate this risk.

Directors noted the benefits conveyed by quantitative monetary easing, and welcomed the Bank of Japan's recent initiative to buy asset-backed securities in order to strengthen the monetary transmission mechanism. Most Directors considered that a more decisive and proactive approach is required to tackle deflation effectively. This could include purchases of a wider range of assets, helping to reflate the economy through asset prices as well as the liquidity channel. Regarding the suggestion to extend asset purchases to foreign currency assets, many Directors were concerned about the related exchange rate effects on trade flows and global imbalances. At the same time, several Directors called attention to the positive impact of a more decisive Japanese monetary policy on global output, and considered that the potential risks to global imbalances related to such purchases were acceptable.

Most Directors considered that the risks to the Bank of Japan's balance sheet arising from extensive purchases of a wider range of assets should be manageable, including through loss sharing arrangements with the government. There was general agreement that it would be desirable to accompany this approach with a clear public communications strategy, including committing to end deflation in a limited time period. Regarding the recommendation that the authorities establish a medium-term inflation target, some Directors saw merit in setting such a target, pointing to its usefulness in anchoring medium-term inflation expectations. A number of Directors, however, cautioned that the credibility of the central bank could be affected if a declared inflation objective were not met, and referred to the lack of effective monetary instruments.

Directors welcomed the authorities' intentions to move toward fiscal consolidation, but cautioned that a substantial medium-term adjustment is needed to put the public debt on a sustainable trajectory and avoid a harmful rise in long-term interest rates. They thought that the adjustment may need to go beyond the official goal of achieving a primary balance by the early 2010s. Achieving fiscal sustainability will require a major reform of the social security system that eliminates its net liabilities in present value terms, with significant adjustments in pension contributions and benefits, along with measures to address the growing costs of the medical insurance system. It was also noted that there might be scope for broadening the personal income tax base, increasing the consumption tax rate, and further reducing public investment. Directors urged the authorities to define a transparent program of sequenced specific measures up front, as this would strengthen the credibility of the medium-term consolidation strategy.

Regarding the near-term stance of fiscal policy, Directors considered that the estimated small cut in the FY2003 structural deficit is broadly appropriate, as it balances the need for fiscal consolidation with the need to protect the still-fragile economic recovery. Looking to FY2004, the expected continued growth should facilitate a stronger push toward consolidation, and signal the government's commitment to the goal of medium-term fiscal sustainability.

Directors encouraged Japan to play a leading role in moving the Doha Round of trade negotiations forward, and to commit to ambitious reductions in agricultural support. Directors welcomed the recent widening of quota- and duty-free access for imports from less developed countries, and encouraged the authorities to take additional steps in that direction.

Directors commended Japan's continued commitment to official development assistance (ODA), observing that Japan remains the second largest ODA provider in absolute terms and that Japan's ODA relative to gross national income exceeds the average for the major industrial countries, notwithstanding its challenging economic situation.

Directors noted recent steps to improve the framework for anti-money laundering and countering the financing of terrorism (AML/CFT), and welcomed Japan's participation in an AML/CFT ROSC.

Japan: Selected Economic Indicators

GDP 1/

Private consumption

Nonresidential investment

Residential investment

Public investment

Public consumption

Stockbuilding (contribution to growth)

Foreign balance (contribution to growth)

Exports of goods and services

Imports of goods and services

GDP deflator

Unemployment rate (period average, percent)

Current account balance

Billions of U.S. dollars

Percent of GDP

General government balances (percent of GDP)

Balance including social security

Balance excluding social security

Structural balance 2/

Base money

20.4 3/

M2 + CDs (period average) 4/

1.8 3/

Bank lending 4/

-4.7 3/

Exchange and interest rates (period average)

Yen/dollar rate

116.5 5/

Real effective exchange rate 6/

106.3 3/

3-month CD rate

0.08 5/

10-year government bond yield

1.67 5/

Sources: Global Insight, Nomura database and IMF staff estimates and projections.

2/ Including social security, excluding bank support.

3/ July 2003.

4/ From April 1998 onward, data reflect the inclusion of foreign banks, foreign trust banks and Shinkin banks in the monetary survey.

5/ September 2, 2003.

6/ Based on normalized unit labor costs; 1990 = 100.

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Authors and Directors

I grew up in Michigan, the older of two kids, but the second-oldest of all of my cousins. Every Thanksgiving we would drive to Cleveland for our family gathering, where I would hear about my older cousin Amruta’s exploits, and a couple years later, reproduce them.

She went to Penn; I went to Stanford. She spent a year living in India, I spent two. Post-graduation she started in management consulting; three years later, I followed suit.

Our paths led us both to San Francisco, but while Amruta got a J.D. and became a law associate, I quit my consulting job, taught myself to code, and became a programmer.

If you ask Amruta, she’ll say that the common thread of McKinsey and Big Law has been learning to operate in tough workplace environments. Her one-on-ones at McKinsey gave her detailed personality feedback; she was told point-blank to focus on her assertiveness.

Amruta was receiving training about how to effectively implement ideas in an organizational context — engaging with stakeholders, overcoming opposition, and so on.

My main job perk, on the other hand, is being able to sit on a couch all day and think. I give substantive status reports once or twice a week, as opposed to multiple times a day in consulting.

Amruta is a knowledge worker who primarily implements her ideas in an organizational context. I am a knowledge worker whose ideas primarily execute, and replicate, themselves in browsers and on servers.

We’ll call Amruta’s type Directors and my type Authors.

Winning friends and influencing people

Directors have ridden two organizational waves to prominence.

The first was the rise of their host environment, the corporation, in the 18th and 19th century. Before then, the only large organizations were the civil service and the military.

Second, in the 20th century, a battle broke out between specialists and generalists to control corporations. And the generalists won, over and over again.  Morgan bought out Carnegie in the ‘00s, the ‘50s marked the ascension of the Whiz Kids, the ‘80s saw the emergence of management consulting and private equity shops, firms premised on generalist ability.

Today emerging tech companies, generally in Silicon Valley, are one of the few areas where specialists retain the upper hand. (see Bezos, Jeff; Page, Larry; and Zuckerberg, Mark).

A recent flashpoint in this battle was the serious consideration of Ford CEO Alan Mulally to be the CEO of Microsoft.

To be effective, Mulally, as one person, would have to able to apply his influence effectively enough to improve the embedded culture and processes of a 200,000-person organization producing products unfamiliar to him.

To hire him, you would have to believe Microsoft’s products are relatively unimportant — widgets, as it were; but that the ability to “steer the ship” was crucial.

It is this system of beliefs that governs the education of Directors; it is a set of beliefs encapsulated in the pages of the HBR and the McKinsey Quarterly, and its successful disciples are able to pave a path through consulting and finance to the VP-level and the C-suite.

Are you in the game or not?

Directors’ aspirations impose several constraints. Two that stand out quickly are tightly regulated entry and a sharp inside/outside distinction.

Tightly regulated entry

There are self-taught programmers. There are no self-taught investment bankers.

Programmers can build ‘toy’ projects that use basically all the same tools and frameworks as they’d actually use in renumerative work.

Investment banking analysts might work in Excel/Powerpoint, but they operate in an organizational context with proprietary client data, client relationships, and firm-transmitted spreadsheet techniques and rigor. These are skills impossible to develop sitting in your living room.

Sharp inside/outside distinction

Another friend who left BCG and is teaching himself to program remarked on the difficulty of giving up his self-image as someone who is Running Things.

Because Directors are so organizationally focused, their boundary distinctions are far more defined by organizational needs than other professions.

Directors must be always in the game — holding a job of a certain type — or they are out of it.  Lifestyle decisions — a year sailing around the world; staying home while the kids are young — will be perceived as Resume Gaps to be explained.

Lean In, the how-to guide for budding Directors, puts it this way: “Don’t put on the brakes. Accelerate. Keep your foot on the gas pedal.”

One review summarized this attitude succinctly: “Sandberg has penned not so much a new Feminine Mystique as an updated Protestant Ethic and the Spirit of Capitalism.”

A broader view of ‘code’

The modern era has seen a rise of Authors along with Directors, albeit due to different technologies.

Consider Homer, author of the Odyssey and Iliad. He had the technology to spread his story (spoken language), but not to direct revenue back to him.

Authors need (1) an environment for their code to run in and (2) a link from their code to themselves — what we’ll call strong replication. Without strong replication (perhaps because the technology doesn’t exist), authors often switch from writing code to performing — becoming a bard.

I’m using the word ‘code’ here in a far broader sense than is typical. Programming code runs on browsers and servers, but there are lots of other things that ‘execute themselves’ that I will group under the rubric of ‘code’:

  • Printed music and books. These can continue to be printed and read indefinitely, by an almost indefinite number of people, without (in theory) the author’s further involvement. Enabling technology: the printing press, copyright law

  • Tim Ferriss’s Muse businesses. These are ongoing, profit-generating concerns, usually drop-shipping goods online, with operations totally outsourced to various customer support personnel. Enabling technology: Moore’s Law, the Internet, e-commerce.

  • Corporations with departed founder: Entrepreneurs who build a corporation until it doesn’t need their supervision, have now created an independent entity in which they own equity, eg, the right to future income streams.  Enabling technology: corporation law, financial markets.

Works that spread fame but not money to their author encapsulate a somewhat weaker link. Baroque musicians were unable to earn fees from the popularity of their music, but the best ones could parlay their fame into patronage or a court position.

In more modern times, we often see Authors supplementing income from low-CPM/low-margin viral content with high-margin in-person bard work.

Musicians go on tour.  Industry blogs hold “money-minting” conferences. And software product businesses upsell with add-on, high-margin consulting services.

The rise of Authors

Many Authors become free agents in the modern economy; others could if they wanted to.

Free agents, living on a constant stream of gigs and contracts, are often sentimental about the flexibility and autonomy their role affords them. One friend, a freelance science writer, laughs that at noon she’s always at home and usually in pajamas.

But it’s useful to think of why this is a difficult choice.  Free agents are typically companies in miniature; they have P&L statements and are responsible for the full stack of functions: marketing, sales, operations, R&D. This can be kind of painful.

Ronald Coase won a Nobel in economics for the observation that organizations are formed when intra-organization coordination costs are lower than external coordination costs. The corollary here is that as e-commerce cuts external coordination costs, that it decreases the need to be associated with a firm.

So in an environment where revenue is chunky and fixed overhead costs are high, individuals should group together into large organizations, ie, join a company.

But the concrete effect of the Internet and Moore’s Law has been to create an environment where revenue can dribble in increments of $8 CPMs or $100 sales, and server costs drop 100x in 10 years.

And now, instead of hunting big animals in groups, we can gather berries and nuts independently.

Organizations with more surface area

Reduced external coordination costs draw individuals out of large organizations to be free agents, but they also have implications for the structures they leave behind.

Increased necessity to interact with the environment is generally bad for the Fortune 500; the effect of the square-cube law is to decrease their surface area to volume ratio.

But even if the organization cannot readily change size, it can change shape — become more like a jellyfish or a sponge than a sphere.

The work practices of the ‘new economy’, even if not widely distributed, seem to reflect this:

Closer engagement with customers: One option, for large organizations, is replacing functional org structures (sales/marketing/R&D) with regional or business-unit org structures. Another for startups is what Steve Blank calls “getting out of the building” — figuring out what to build by relentlessly talking to customers.

Closer engagement with producer/business ecosystem: Serious hackathon contests, whether structured like Salesforce $1M prize or like Netflix’s $1M prize, necessitate making one’s data and functionality legible to and interactive with the outside world. App platforms and APIs (interfaces providing access to an application’s data) have similar effect.

More modular internal structures: Remote working means a decreased shared internal context, and greater likelihood for workers to look externally for best practices.

These organizational practices form a sort of environmental superstructure for individual Authors.

Continuing our marine analogy, we could say that these structures are like surfaces, and Authors and other free agents  are algae that grow on the surfaces.

If you can solve problems well on Kaggle, you can likely find consulting gigs. Given the Google Maps API, you can build something else on top of it. Get out of the building, and you can probably support yourself by meeting your customers’ needs.

The most important things need Director skills

So the new economy is shifting the Author / Director balance of power towards Authors; and Authors have some lifestyle benefits not available to Directors.

But I often wonder if my cousin Amruta gets something important that my fellow Authors and I are missing.

If you spend a lot of time listening to the phone calls of biz-dev guys, or the meetings of upper management, you tend to hear a rich vocabulary of intentions, feelings, and relationships. If you spend a lot of time listening to engineers’ standups, you tend to hear intricate descriptions of systems and their functionality.

The careers of Directors train them in ethos, logos, and pathos about equally; the careers of engineer Authors train them primarily in logos.

Let’s think about parenting, probably the most universal moral playing field out there. We’ll assume, reasonably, that the values transmitted in the workplace play a strong role in the values being transmitted in the home.

Good parenting involves ethos (“trust me”), pathos (“I know this is something you really want…”), and logos (“we do it this way because…”).

A parenting style that is overly logos-heavy, on the other hand, faces a couple drawbacks.

First, it is less cognizant of the power of example (that is related to ethos). Bad examples tend to create more deeply embedded problems than bad values, because children react more unconsciously to behavior patterns than to stated values.

Second, it has the potential to be, as Kevin Simler put it, overly prickly. This family of 12 children, governed by 28 explicit bullet-pointed paragraphs of rules, is an extreme example here.

Extending beyond parenting into the more general case, many of the same conclusions hold.

If I wish to influence others for good, using only logos will restrict my audience and cripple my influence. Charles Murray has noted that the college-educated meritocracy already has difficulty articulating its values to those outside its sphere.

As technical systems and frameworks become increasingly important, the need for Authors to build on top of them is paramount; yet I can’t help but feel a certain amount of sadness about the tradeoff.

Thanks to Venkatesh, Randy Lubin, Mike Travers, Kyle Mathews, and Kartik Agaram for reading over drafts of this essay.

About Sam Bhagwat

  1. I’m an engineer (of sorts) in a 90 thousand employee multi-billion dollar privately owned company. To be hired by this company in any role from the factory to the IT department you have to pitch a business plan successfully to your interviewers. Start as you mean to go on because every day is an influence. In this 90 thousand employee organisation, there is only one successful company-wide system or process and that’s the one to manage people’s objectives and even that is often ignored. A sea of people, working for and against each other. Yet somehow it works and is competitive in the marketplace. Being able to do something is worth jack. Having done something is worth jack. It’s an Author’s nightmare but it provides a lot of resources to do cool stuff and it sure has trained me to think like a Director.

    To observe the big fish in this sea is to see Constantine-like theatrical changes of mind, Bismark-like networks of stakeholders and factions go to smiling war with each other.

    …and we’re hiring. :)

  2. One aspect of the distinction you didn’t get to is measurability. Not in an artificial metrics sense, but natural sense. Author work is by nature more measurable, while director work and director makework are often hard to tell apart.

    One consequence of this that I’ve noticed is that authors are less sensitive to pay as a measure of status than directors, whether they operate in freelance or paycheck ways.

    • Or job title.

      Authors don’t need any particular job title. Their body of work is what brings them recognition. To directors, job title is everything, more important even than pay, and much ethos/pathos is required just to sustain it.

  3. Many jokes are made about herding cats, but on a serious note, do you get the impression your cat is herding you? I certainly do; if I am anywhere near the kitchen, he does a thing I would call “Managing by Getting In the Way”. Many human managers instinctively do the same thing, and I’m considering writing a book by that title. I would definitely categorize this as director behaviour, and generalist (despite the fact that in cats it is always exercised to the same end — they just happen to only have one end, but clearly its applications are more general than that — and I definitely can’t conceive of my cat as an author.


Journal of Applied Physiology

Hypoxia recruits intrapulmonary arteriovenous pathways in intact rats but not isolated rat lungs

Melissa L. Bates, Brendan R. Fulmer, Emily T. Farrell, Alyssa Drezdon, David F. Pegelow, Robert L. Conhaim, Marlowe W. Eldridge

Intrapulmonary arteriovenous anastomoses (IPAVS) directly connect the arterial and venous circulations in the lung, bypassing the capillary network. Here, we used solid, latex microspheres and isolated rat lung and intact, spontaneously breathing rat models to test the hypothesis that IPAVS are recruited by alveolar hypoxia. We found that hypoxia recruits IPAVS in the intact rat, but not the isolated lung. IPAVS are at least 70 μm in the rat and, interestingly, appear to be recruited when the mixed venous Po2 falls below 22 mmHg. These data provide evidence that large-diameter, direct arteriovenous connections exist in the lung and are recruitable by hypoxia in the intact animal.

  • arteriovenous anastamoses
  • hypoxia
  • intrapulmonary shunts
  • lung
  • microspheres

inducible intrapulmonary arteriovenous anastamoses (IPAVS) are large-diameter pathways that connect the pulmonary arterial and venous circulations, bypassing the lung's capillaries. Studies using saline contrast echocardiography demonstrate that IPAVS are closed in healthy, adult humans, breathing room air [fractional inspired O2 (FiO2) = 0.21] at rest (7, 8, 15, 18, 19). However, they are recruited with exercise at ≥60% of maximal exercise capacity in most individuals (7). Indeed, transpulmonary bubble passage has been observed in ∼90% of participants tested while performing maximal exercise in our laboratory. Exercise with hypoxia (FiO2 = 0.12) causes the pathways to be recruited at lower workloads (18) than with normoxia and IPAVS can be recruited at rest in many individuals breathing an FiO2 < 0.10 (15). Hyperoxia apparently closes these pathways, preventing the passage of saline bubble contrast, even with high-intensity exercise (19).

However, saline bubble echocardiography is limited in that it provides only qualitative measurements of IPAVS recruitment (12). Furthermore, saline contrast yields no information about IPAVS diameter. Thus, although saline contrast is a useful, minimally invasive tool for making repeated measures of IPAVS recruitment in humans, there is an additional need for a model using solid particles of known diameter to investigate the mechanism of IPAVS recruitment and their impact on gas exchange. We have previously used 25-μm solid microspheres in dogs to verify the recruitment of IPAVS during normoxic exercise. Here, we aimed to establish a rat model of IPAVS recruitment in hypoxia and to determine the diameter of IPAVS in this species.

We conducted four experiments using our previously described fluorescent microsphere method to test the hypothesis that IPAVS > 50 μm are recruited by alveolar hypoxia in the rat. In the first experiment, we ventilated isolated rat lungs with normoxic (FiO2 = 0.21) or hypoxic gas (FiO2 = 0.08) and assessed whether large-diameter microspheres traverse the lung under each condition. When we found that hypoxia did not recruit IPAVS in the isolated rat lung, we conducted a second experiment in which we exposed intact, anesthetized, spontaneously breathing rats to normoxic or hypoxic gas (FiO2 = 0.12) and found evidence of transpulmonary microsphere passage in hypoxia. In the third and fourth experiments, we varied the microsphere size to determine IPAVS diameter and investigated the effect of varying the FiO2 on IPAVS recruitment.

Male Sprague-Dawley (250–350 g) rats (Harlan Laboratories) were maintained in standard animal housing on a 12:12-h light-dark cycle and offered water and chow ad libitum. All protocols were approved by the institutional animal care and use committee at the University of Wisconsin-Madison. Each of the experiments described in detail in subsequent sections used the same general approach. Isolated lungs or intact rats were exposed to normoxic or hypoxic gas for 5 min with IPAVS recruitment assessed by quantifying the transpulmonary passage of microspheres. Blood gases were always obtained before the injection of microspheres. Additionally, we dissected, examined, and probed the atrial and ventricular septa of all rats reported in this manuscript. Two rats with evidence of an atrial-level shunt were excluded from our data set. Careful postmortem analysis of the animals included in our data set revealed no intracardiac conduit, including a patent foramen ovale, that could allow for transcardiac microsphere passage.

Experiment 1: effect of alveolar hypoxia on IPAVS recruitment in isolated lungs.

Lungs were isolated and prepared using previously well-described methods (5, 6, 20, 32). Briefly, rats were anesthetized with ketamine and xylazine (50–100 mg/kg and 5 mg/kg ip) and secured supine. A polyethylene catheter was placed in the femoral vein and infused with heparin (6,000 U/kg) to prevent lung thrombus formation during isolation. The femoral artery was then cut and blood was flushed from the animal by perfusing 10 ml isotonic phosphate-buffered saline (PBS, pH = 7.4) into the femoral vein. The trachea was isolated, cannulated with polyethylene tubing, and the lungs inflated with 5 ml of air. A midline sternotomy was performed, the chest wall removed, and fluid-filled polyethylene catheters were placed in the pulmonary artery and left atrium. Lungs were left in situ in the thorax and 3 ml PBS was added to the chest cavity to prevent dehydration and to minimize friction between the lung and chest wall. The lungs were mechanically ventilated with FiO2 = 0.08 (n = 5) or 0.21 (n = 4), balance N2, 30–45 times per minute (3–4 ml/inflation) to a peak inflation pressure of 15 cmH2O with 5 cmH2O end-expiratory pressure.

The pulmonary arterial catheter was connected to a continuous-flow reservoir system containing 5% albumin in heparinized PBS (1,000 U/l, pH = 7.4). This reservoir was supplied by a pump and had an overflow outlet so that the height of the fluid column could be maintained at a constant level. The perfusion pressure was thus determined by the height of the fluid column above the pulmonary artery, which we set to 20 cmH2O. The left atrial catheter was maintained at the level of the atrium so that the outlet pressure equaled 0 cmH2O and the entire left atrial effluent was collected. Lungs were ventilated and perfused for 5 min before beginning our study protocol.

One million 15 ± 12% μm green fluorescent microspheres (Duke Scientific) were suspended in 4 ml PBS as previously described (20) and injected in four 1-ml boluses (1/4 of 4 ml with 250,000 microspheres per bolus) via an injection port in the pulmonary artery catheter. Microspheres were injected in multiple boluses over 20 min, instead of as a single injection, to minimize the risk of microsphere clumping in large-diameter vessels. The entire left atrial effluent was vortexed and vacuum filtered through a filter with 8-μm pores (Millipore, Billerica, MA). Microspheres trapped in the filters were imaged using a fluorescent microscope and counted.

Experiment 2: effect of alveolar hypoxia on IPAVS recruitment in intact rats.

Rats were anesthetized with ketamine and xylazine (50–100 mg/kg and 5 mg/kg ip) and placed on an electric homeothermic blanket. Body temperature was measured with a rectal probe and the blanket was adjusted to maintain a body temperature of 36–38°C. Once a surgical plane of anesthesia was verified, the neck was exposed and the right carotid artery and jugular vein were isolated. A 0.5-mm microtip pressure-volume catheter (Millar Instruments, MPVS Ultra and SPR-839, Houston, TX) was introduced via the carotid artery into the left ventricle to measure left ventricular pressure and volumes. Pressure-volume data were acquired with a PowerLab data acquisition device and analyzed using the LabChart software package (AD Instruments, Colorado Springs, CO) (24). Before each use, the catheter was calibrated according to the manufacturer's instructions using a sample of each animal's own blood. The electronic pressure calibration was verified before use (Veri-Cal, Utah Medical Products, Midvale, UT).

To measure right ventricular pressure, a Tygon catheter (0.010 in. ID, 0.030 in. OD) was connected to a pressure transducer (Hospira, Lake Forest, IL) and introduced into the right ventricle via the jugular vein. The final location of the catheter was assessed by monitoring the pressure waveform during placement and was verified postmortem. A second polyethylene catheter was introduced into the superior vena cava via the same jugular vein for microsphere injection. A third polyethylene catheter was placed in the femoral artery for blood gas analysis. Rats were then sealed into a custom-built Plexiglas chamber that was equipped with inlet and outlet ports that were used to flush the condition gas through the chamber. The FiO2 in the chamber was monitored continuously at the outlet port (MiniOx I, MSA, Cranberry Township, PA). The chamber was flushed (15 l/min) with FiO2 = 0.12 or 0.21, balance N2, until the inlet and outlet FiO2 was equal. An FiO2 of 0.12 was chosen because it resulted in an alveolar Po2 (PaO2) similar to that of the isolated lungs ventilated with FiO2 = 0.08 (PaO2 = 57 mmHg in isolated lungs vs. 54 mmHg in intact rats). PaO2 in intact rats was estimated from the alveolar gas equation, based on the assumption that arterial Pco2 (PaCO2) equaled that in alveolar gas and that the respiratory quotient = 0.8.

After a 5-min exposure to either 12 (n = 6) or 21% O2 (n = 5), 1 ml of arterial blood was drawn from the femoral arterial catheter for blood gas analysis. Samples were run in duplicate (pHOx Basic, Nova Biomedical, Waltham, MA) and corrected for body temperature. A three-point calibration was done daily using manufacturer-supplied control solutions with known values of Po2, Pco2, and pH. One million 15-μm green fluorescent microspheres were then injected into the superior vena cava and the rat was euthanized by exsanguination. The kidneys were removed, embedded in Tissue-Tek, and flash-frozen in liquid nitrogen. Samples were stored at −20°C until analysis.

A single kidney was chosen at random from each intact rat studied and sliced into sections four times the thickness of the microspheres contained in the tissue. We found that this thickness allowed the microspheres to be easily visualized and that broken or damaged microspheres were seen rarely. The sections were placed on slides, imaged with a fluorescent microscope, and the number of microspheres in each slice was quantified. Every slice was imaged and counted and <5% of the slices were lost or damaged during the sectioning process. To ensure that we had accurately counted the number of microspheres in the kidney slices, we counted the front and back of 10% of the slices and found near-perfect agreement (±1 microsphere).

Experiment 3: assessment of IPAVS size.

Under anesthesia, a polyethylene catheter was placed in the femoral artery for blood gas analysis and femoral vein for microsphere injection. The rat was then placed in the previously described Plexiglas chamber and exposed to FiO2 = 0.12. After 5 min, blood gases were drawn to verify that the rat was hypoxemic. Each rat received an injection of one million microspheres of a single size (10 μm ± 18%, 25 μm ± 12%, 50 μm ± 12%, or 70 μm ± 7%, n = 4 each group, total n = 16) via the femoral catheter. Each rat received an injection of a single microsphere size. The rat was then euthanized by exsanguination and the kidneys were collected and analyzed as described.

Experiment 4: relation between FiO2 and IPAVS recruitment.

Rats were instrumented with left heart, right heart, femoral artery, and superior vena cava catheters as described. They were then placed in the Plexiglas chamber and the chamber was ventilated such that each rat was exposed to a single FiO2 within the range of 0.03–0.21 (n = 24 total). Blood was drawn from the right ventricular and femoral arterial catheters (1 ml total volume) and blood gases were analyzed as described. One million 25-μm microspheres were injected into the superior vena cava catheter. The animals were euthanized and the kidneys were collected and analyzed as described.

Data analysis.

Hemodynamic and blood gas data were analyzed using a Student's t-test and significance set at P < 0.05 with a Bonferroni correction to account for multiple comparisons. The effect of oxygen tension on microsphere passage was assessed using a nonparametric Mann-Whitney test with significance set at P < 0.05 (Minitab, State College, PA). Linear regression was used to evaluate the relation between microsphere passage and FiO2, PvO2, and PaO2. Data are reported as means ± SD.

Experiment 1: effect of alveolar hypoxia on IPAVS recruitment (isolated lungs).

The number of microspheres found in the venous effluent of isolated rat lungs with normoxic and hypoxic ventilation was equal and trivial (78 ± 62 vs. 61 ± 46, P = 0.90), translating to mean transpulmonary microsphere passage <0.01% (Table 1). Perfusate flow was higher in normoxia ventilated isolated lungs (8.9 ± 1.3 ml/min) than hypoxia ventilated lungs (5.1 ± 1.3 ml/min, P = 0.005) and tended to decline, although not significantly, as a result of the injection of 1 × 106 microspheres (7.5 ± 1.5 ml/min in normoxia, P = 0.16 vs. 2.8 ± 1.8 ml/min in hypoxia, P = 0.08).

View this table:
Table 1.

The effect of fractional inspired oxygen on the transpulmonary passage of 15-μm microspheres in isolated rat lungs

Experiment 2: effect of alveolar hypoxia on IPAVS recruitment (intact rats).

As expected, hypoxia (FiO2 = 0.12) depressed arterial Po2 relative to normoxia (28.8 ± 6.9 vs. 65.4 ± 4.4 mmHg, P < 0.001), although rats exposed to normoxia still demonstrated arterial hypoxemia that may have been caused by regional lung atelectasis in these spontaneously breathing animals. There was no difference in arterial Pco2 (23.8 ± 7.7 vs. 28.1 ± 7.7 mmHg, P = 0.43) or pH (7.41 ± 0.19 vs. 7.38 ± 0.15, P = 0.79). Hypoxia increased the number of 15-μm microspheres that bypassed the pulmonary circulation and lodged in the kidney (0 ± 1 vs. 1,119 ± 1,925, P = 0.008) (see Table 2). More than 100 microspheres were observed in the single kidneys of five of six rats exposed to hypoxia. Two microspheres were observed in the kidney of only a single rat exposed to normoxia. No microspheres were observed in the kidneys of the remaining four rats. Again, we note the passage of 100 microspheres as important because, assuming the kidney receives 10% of the cardiac output, this translates to 0.1% of the microspheres having bypassed the lung.

View this table:
Table 2.

Number of 15-μm microspheres found in the kidneys of intact, spontaneously breathing rats exposed to normoxia or hypoxia

The effects of hypoxia and microsphere injection on cardiopulmonary hemodynamics are given in Table 3. As expected, hypoxia elevated the right ventricular systolic pressure and, consequently, the total pulmonary vascular resistance relative to normoxia. Rats exposed to hypoxia demonstrated no hemodynamic changes in response to microsphere injection. Microsphere injection in normoxia caused a transient 10-mmHg increase in right ventricular systolic pressure (P = 0.005) that resolved at the termination of the injection, but no other hemodynamic changes were noted.

View this table:
Table 3.

Right heart pressure and cardiac output in intact, spontaneously breathing rats exposed to normoxia (n = 5) or hypoxia n = 6)

Experiment 3: assessment of IPAVS size.

More than 100 microspheres were found in the single kidney of two of four hypoxemic rats injected with 10-μm microspheres (79 ± 93), five of six rats injected with 15-μm microspheres (1,119 ± 1,925, data from experiment 2), three of four rats injected with 25-μm microspheres (4,979 ± 5,815), three of four rats injected with 50-μm microspheres (4,641 ± 6,913), and four of four rats injected with 70-μm microspheres (637 ± 801) (Fig. 1A). The injection of 70-μm microspheres within the range of microsphere numbers that could be injected reproducibly (2.5 × 105 to 2 × 106) resulted in death within 5 min of injection. For that reason, larger sizes were not attempted in intact animals. Although the mean number of microspheres lodged in the kidney appears higher for the 25- and 50-μm spheres, the SD is also quite high. The higher mean is the result of one rat in each group with a very large number of microspheres (>10,000) and one rat in each group with <100 microspheres. An ANOVA revealed no overall effect of sphere size on the number of microspheres lodged in the kidney (P = 0.27). Therefore, data were pooled and are shown in Fig. 1B. Assuming that the each kidney receives 10% of the cardiac output, and that this is unchanged by hypoxia, this translates to 2.2 ± 4.1% of the microspheres having bypassed the pulmonary circulation in the hypoxic condition. This is certainly an underestimation given that exposure to hypoxia decreases the renal blood flow ∼40% in the anesthetized rat (22).

Fig. 1.

Number of microspheres observed in the kidney as a function of microsphere size (A) and distribution of transpulmonary microsphere passage (B) (n = 22). Transpulmonary microsphere passage was observed in 17/22 rats and microsphere size was not related to the number of microspheres found in the kidney (P = 0.27). In the total population, 2,170 ± 4,118 microspheres were found in the kidney.

Experiment 4: relation between FiO2 and IPAVS recruitment.

As expected, PaO2 (R2 = 0.88, P < 0.001), PvO2 (R2 = 0.52, P < 0.001), and PaCO2 (R2 = 0.54, P < 0.001) decreased with decreasing FiO2. However, decreasing FiO2 had no effect on PvCO2 (R2 = 0.07, P = 0.20). Very few 25-μm microspheres were found in the kidneys of rats with PaO2 > 30 mmHg and PvO2 > 22 mmHg (5 ± 3 microspheres, n = 16). However, more than 100 microspheres were found in the kidneys of six of eight rats with PaO2 < 30 mmHg and PvO2 < 22 mmHg (966 ± 529, P < 0.001) (see Fig. 2). There was no linear correlation between the number of microspheres found in the kidneys of hypoxic rats and FiO2, PvO2, or PaO2 (r2 < 0.10 and P > 0.05 for each comparison).

Fig. 2.

Number of 25-μm microspheres traversing the pulmonary circulation and lodging in the kidney in rats, divided based on the venous partial pressure of oxygen (PvO2). More than 100 microspheres were found in the kidneys of animals with PvO2 < 22 mmHg (n = 8, P < 0.001). Transpulmonary passage of microspheres was not seen in rats with PvO2 > 22 mmHg (n = 16).

We postulated that alveolar hypoxia would be sufficient to recruit IPAVS in isolated rat lungs and intact rats. Surprisingly, even a severe hypoxic stress that routinely recruits IPAVS in humans failed to recruit IPAVS in isolated lungs. This apparent negative finding, however, may provide insight into the anatomic location or regulation of IPAVS in the rat. In the intact rat, we found that hypoxia recruits IPAVS when PaO2 was <30 mmHg and PvO2 was <22 mmHg. Further, we show that IPAVS are at least 70 μm in diameter.

Why does hypoxia fail to recruit IPAVS in the isolated rat lung?

As we have done previously (32), we used both isolated lungs and intact animals to investigate IPAVS recruitment. We found transpulmonary microsphere passage in isolated lungs ventilated with normoxia, although the number of traversing microspheres was very low (0.008%). This is similar to our findings in baboon (0.01%), human (0.06%), and dog lungs (0.001%) (20, 32). Microsphere passage was not enhanced by hypoxia. There are several key differences between the intact animal and isolated lung that may explain our findings.

The lack of IPAVS recruitment in the isolated lung may provide clues about the anatomic location of these pathways. The isolated lung is perfused exclusively between the pulmonary artery and left atrium and lacks an intact bronchial circulation. Although we have generally referred to these pathways as “intrapulmonary” arteriovenous pathways, they may contain an intrabronchial component. The bronchial circulation contains both pre- and postcapillary anastomoses to the pulmonary circulation (30, 34) and the short, muscular Sperr arteries that anastomose the pulmonary arteries to the bronchial arteries may provide a site of active control. These connections are 35–100 μm in diameter in the neonatal lung and appear to functionally close after birth. They remain present in the adult lung and it is hypothesized that there may be physiological or pathological conditions that could lead to their reopening (10).

It is also possible that there are factors missing from the isolated lung that are necessary for IPAVS recruitment. For example, the sympathetic nervous system is activated by both exercise and hypoxia, and catecholamine-mediated vasodilation could explain IPAVS recruitment in both of these conditions. In dogs and humans, epinephrine infusion causes intrapulmonary shunting. This hypoxemia is reduced by 100% O2 breathing or propranolol infusion (2, 3). Furthermore, epinephrine infusion causes the transpulmonary passage of albumin microspheres in the dog (23). We have noted the passage of albumin macroaggregates in exercising humans and the cessation of transpulmonary bubble passage with 100% O2 breathing (17, 19). If a functional sympathetic nervous system is required, hypoxia would not recruit IPAVS in our isolated lung model that lacks innervation and circulating humoral factors.

As in our previous studies, the isolated lungs in these experiments were positive-pressure ventilated and perfused in situ with a room temperature 5% albumin solution that was exposed to the ambient environment. This albumin solution has a high Po2, low Pco2, and nonphysiological temperature. It is possible that these nonphysiological conditions prevented IPAVS recruitment in the isolated lung. Each of these variables may have an independent effect on IPAVS recruitment.

What recruits intrapulmonary arteriovenous anastomoses with hypoxia and exercise?

Although the original purpose of these experiments was to test the question of whether exposure to a hypoxia recruits IPAVS, our findings in the intact rat lend additional insight into the mechanism by which IPAVS are recruited. During exercise, especially at workloads where we have observed IPAVS recruitment, PvCO2 is elevated. However, PvCO2 did not change with hypoxia exposure in our experiments, providing evidence that elevated PvCO2 is not required for IPAVS recruitment. Also, the fact that the cardiac output was not elevated by hypoxia in our experiments suggests that increased pulmonary blood flow is also not required for IPAVS recruitment.

As expected, we did observe elevations in pulmonary vascular pressure with hypoxia exposure and cannot rule out the possibility that IPAVS recruitment is mediated by elevations in pulmonary artery pressure. Evidence in humans in support of pressure-mediated recruitment of these pathways is conflicting. For example, Stickland et al. (33) found that elevating pulmonary artery pressure had minimal impact on IPAVS recruitment in exercising humans. Laurie et al. (15) also found no causal relationship between the onset of IPAVS recruitment and ultrasound-assessed pulmonary artery pressure in human volunteers exposed to hypoxia. However, lower pulmonary artery pressures have been observed in exercising humans with evidence of IPAVS recruitment compared with those without (14).

We examined the effect of altering FiO2 on IPAVS recruitment and, as expected, arterial Po2 declined as a function of decreasing FiO2 and, interestingly, IPAVS recruitment occurred only with PaO2 < 30 mmHg and PvO2 < 22 mmHg. This PaO2 is much lower than those observed in humans with transpulmonary bubble passage (18) and, although we cannot rule out the potential confounding effect of anesthesia, we speculate that the signal for IPAVS recruitment may be on the venous side of the circulation. It is interesting that the PvO2 observed in our study when IPAVS were recruited is similar to the PvO2 during exercise and simulated altitude (27), although direct measurements of PvO2 and IPAVS recruitment have not been made simultaneously in humans or animals. Future studies in large-animal models, where the venous and arterial oxygen tensions can be isolated and controlled individually, would be valuable in testing this mechanism further.

How large are intrapulmonary arteriovenous anastomoses?

We used 15-μm microspheres to assess the fraction of blood flow bypassing the pulmonary capillary bed and traveling through direct intrapulmonary arteriovenous anastomoses. The rationale for choosing this size microsphere was based on data suggesting that greatest mean capillary diameter observed in greyhound lungs perfused at 37–74 mmHg is 6.5 μm and the largest capillaries observed were no larger than 13 μm (9). Still, we appreciate that one possible interpretation of the transpulmonary passage of 15-μm microspheres is passage through distended corner capillaries ≈20 μm (9, 28, 29). Rosenweig et al. (29) demonstrated the these corner capillaries are extensively recruited in zone 1, allowing arterially perfused dye to enter the pulmonary veins. To verify that we were observing the recruitment of true arteriovenous anastamoses and not the passage of microspheres through corner capillaries, we tested microspheres up to 70-μm diameter in intact rats exposed to hypoxia. The Strahler model of the rat vascular tree places 70-μm vessels at the level of fifth-generation pulmonary arteries (13). Assuming a corner capillary diameter of 20 μm, a 2% change in diameter per mmHg increase in capillary transmural pressure (11, 16, 26), and an initial transmural pressure equal to half the pulmonary artery (20 mmHg) and left atrial pressures (5 mmHg), 140 mmHg transmural pressure would be required to distend a corner capillary sufficiently to allow the passage of a 70-μm particle. Distension of a 6.5-μm alveolar capillary to 70 μm would require 488 mmHg transmural pressure. Thus it seems impossible that these large-diameter microspheres are passing through distended capillaries.

What are the clinical and pathological consequences of recruiting intrapulmonary arteriovenous anastomoses?

The ability to modulate IPAVS may have important clinical consequences. In addition to its role in gas exchange, the lung is an important biological filter and IPAVS provide a route by which large-diameter particles can bypass this filter. Fifty percent of pediatric strokes are cryptogenic, occurring in the absence of hypercoagulative state, trauma, infection, or apparent cardiovascular disease (4, 21). Paradoxical embolism (an arterial embolism caused by a thrombus with a venous origin) has been considered as a possible mechanism, but only 45% of stroke patients have a patent foramen ovale to allow these thrombi to bypass the lung filter (1). Direct arteriovenous connections may serve as an alternative pathway to allow potentially dangerous blood clots, air bubbles, fat particles, or parasites to bypass the lung filter and reach the brain. It is particularly relevant that emboli similar in size to our 70-μm microspheres cause function performance deficits when injected into the cerebral circulation in rats (25). We examined the brains of a small subset of rats and found cerebral embolization by our microspheres (Fig. 3).

Fig. 3.

Transverse section through the base of a rat brain. One million 15 (green)- and 33 (red)-μm spheres were injected into the superior vena cava, followed by 100 μl Evan's Blue dye to label the remaining patent vasculature. The brain was removed, embedded in Tissue Tek, sliced, and imaged confocally. Note that embolization by the 33-μm microsphere has disrupted perfusion.

We demonstrate that IPAVS at least 70 μm in diameter are recruited by hypoxia in the intact rat. These findings support previous observations made in human research participants. Microspheres do not traverse the isolated hypoxic lung, but are found in the systemic circulation of intact, hypoxemic rats. Although the mechanism of recruitment remains unknown, microsphere passage is observed at PvO2 < 22 mmHg, suggesting a role for the mixed venous Po2 in IPAVS recruitment.

This work was supported by grants from the National Institutes of Health (5R01-HL-086897 and 5T32-HL-007654) and a postdoctoral fellowship from the American Heart Association.

Author contributions: M.L.B., B.R.F., E.T.F., A.D., D.F.P., R.L.C., and M.W.E. conception and design of research; M.L.B., B.R.F., A.D., and D.F.P. performed experiments; M.L.B., B.R.F., A.D., and M.W.E. analyzed data; M.L.B., E.T.F., D.F.P., R.L.C., and M.W.E. interpreted results of experiments; M.L.B. and M.W.E. prepared figures; M.L.B. and M.W.E. drafted manuscript; M.L.B., B.R.F., E.T.F., A.D., D.F.P., R.L.C., and M.W.E. edited and revised manuscript; M.L.B., B.R.F., E.T.F., A.D., D.F.P., R.L.C., and M.W.E. approved final version of manuscript.

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View Abstract


January 28, 2011

Area: 329,847 sq. km. (127,315 sq. mi.); slightly larger than New Mexico.
Cities: Capital--Kuala Lumpur. Other cities--Penang, Ipoh, Malacca, Johor Baru, Shah Alam, Klang, Kuching, Kota Kinabalu, Kota Baru, Kuala Terengganu, Miri, Petaling Jaya.
Terrain: Coastal plains and interior, jungle-covered mountains. The South China Sea separates peninsular Malaysia from East Malaysia on Borneo.
Climate: Tropical.

Nationality: Noun and adjective--Malaysian(s).
Population (2010): 28.3 million.
Annual population growth rate: 1.7%.
Ethnic groups: Malay 53.3%, Chinese 26.0%, indigenous 11.8%, Indian 7.7%, others 1.2%.
Religions: Islam (60.4%), Buddhism (19.2%), Christianity (9.1%), Hinduism (6.3%), other/none (5.0%).
Languages: Bahasa Melayu (official), Chinese (various dialects), English, Tamil, indigenous.
Education: Years compulsory--6. Attendance--90.1% (primary), 60.0% (secondary). Literacy--93.5%.
Health: Infant mortality rate (2007)--6.7/1,000. Life expectancy (2007)--female 76.4 yrs., male 71.9 yrs.
Work force (10.89 million, 2007): Services--57%; industry--28% (manufacturing--19%, mining and construction--9%); agriculture--15%.

Type: Federal parliamentary democracy with a constitutional monarch.
Independence: August 31, 1957. (Malaya, which is now peninsular Malaysia, became independent in 1957. In 1963 Malaya, Sabah, Sarawak, and Singapore formed Malaysia. Singapore became an independent country in 1965.)
Constitution: 1957.
Subdivisions: 13 states and three federal territories (Kuala Lumpur, Labuan Island, Putrajaya federal administrative territory). Each state has an assembly and government headed by a chief minister. Nine of these states have hereditary rulers, generally titled "sultans," while the remaining four have appointed governors in counterpart positions.
Branches: Executive--Yang di-Pertuan Agong (head of state and customarily referred to as the king; has ceremonial duties), prime minister (head of government), cabinet. Legislative--bicameral parliament, comprising 70-member Senate (26 elected by the 13 state assemblies, 44 appointed by the king on the prime minister's recommendation) and 222-member House of Representatives (elected from single-member districts). Judicial--Federal Court, Court of Appeals, high courts, session's courts, magistrate's courts, and juvenile courts. Sharia courts hear cases on certain matters involving Muslims only.
Political parties: Barisan Nasional (National Front)--a coalition comprising the United Malays National Organization (UMNO) and 12 other parties, most of which are ethnically based; Democratic Action Party (DAP); Parti Islam se Malaysia (PAS); Parti Keadilan Rakyat Malaysia (PKR). There are more than 30 registered political parties, including the foregoing, not all of which are represented in the federal parliament.
Suffrage: Universal adult (voting age 21).

Economy (2009)
Nominal GDP: $191.5 billion.
Annual real GDP growth rate: 5.9% (2006); 6.3% (2007); 4.6% (2008); -1.7% (2009); 7.0% (government estimate for 2010).
Nominal per capita income (GNI): $6,897.
Natural resources: Petroleum, liquefied natural gas (LNG), tin, minerals.
Agricultural products: Palm oil, rubber, timber, cocoa, rice, tropical fruit, fish, coconut.
Industry: Types--electronics, electrical products, chemicals, food and beverages, metal and machine products, apparel.
Trade: Merchandise exports--$180.8 billion: electronic products, machinery, liquid natural gas, petroleum and petroleum products, telecom equipment. Major markets--Singapore 14.0%, China 12.2%, U.S. 11.0%, Japan 9.8%. Merchandise imports--$142.1 billion: electronic products, machinery, machinery parts and apparatus, petroleum and petroleum products. Major suppliers--China 14.0%, Japan 12.5%, U.S. 11.2%, Singapore 11.1%.

Malaysia's multi-racial society contains many ethnic groups. Malays comprise a majority of just over 50%. By constitutional definition, all Malays are Muslim. About a quarter of the population is ethnic Chinese, a group which historically played an important role in trade and business. Malaysians of Indian descent comprise about 7% of the population and include Hindus, Muslims, Buddhists, and Christians. Non-Malay indigenous groups combine to make up approximately 11% of the population.

Population density is highest in peninsular Malaysia, home to some 20 million of the country's 28 million inhabitants. The rest live on the Malaysian portion of the island of Borneo in the large but less densely-populated states of Sabah and Sarawak. More than half of Sarawak's residents and about two-thirds of Sabah's are from indigenous groups.

Drawn by this rich trade, a Portuguese fleet conquered Malacca in 1511, marking the beginning of European expansion in Southeast Asia. The Dutch ousted the Portuguese from Malacca in 1641. The British obtained the island of Penang in 1786 and temporarily controlled Malacca with Dutch acquiescence from 1795 to 1818 to prevent it from falling to the French during the Napoleonic war. The British gained lasting possession of Malacca from the Dutch in 1824, through the Anglo-Dutch treaty, in exchange for territory on the island of Sumatra in what is today Indonesia.

In 1826, the British settlements of Malacca, Penang, and Singapore were combined to form the Colony of the Straits Settlements. From these strongholds, in the 19th and early 20th centuries the British established protectorates over the Malay sultanates on the peninsula. During their rule the British developed large-scale rubber and tin production and established a system of public administration. British control was interrupted by World War II and the Japanese occupation from 1941 to 1945.

Popular sentiment for independence swelled during and after the war. The territories of peninsular Malaysia joined together to form the Federation of Malaya in 1948 and eventually negotiated independence from the British in 1957. Tunku Abdul Rahman became the first prime minister. In 1963 the British colonies of Singapore, Sarawak, and Sabah joined the Federation, which was renamed Malaysia. Singapore's membership was short-lived, however; it left in 1965 and became an independent republic.

Neighboring Indonesia objected to the formation of Malaysia and began a program of economic, political, diplomatic, and military "confrontation" against the new country in 1963, which ended only after the fall of Indonesia's President Sukarno in 1966. Internally, local communists, nearly all Chinese, carried out a long, bitter insurgency both before and after independence, prompting the imposition of a state of emergency from 1948 to 1960. Small bands of guerrillas remained in bases along the rugged border with southern Thailand, occasionally entering northern Malaysia. These guerrillas finally signed a peace accord with the Malaysian Government in December 1989. A separate, small-scale communist insurgency that began in the mid-1960s in Sarawak also ended with the signing of a peace accord in October 1990.

Malaysia is a constitutional monarchy, nominally headed by the Yang di-Pertuan Agong, customarily referred to as the king. The king is elected for 5-year terms from among the nine sultans of the peninsular Malaysian states. The king also is the leader of the Islamic faith in Malaysia.

The bicameral parliament consists of the Senate (Dewan Negara) and the House of Representatives (Dewan Rakyat). All 70 Senate members sit for 3-year terms, which are normally extended for an additional 3 years; 26 are elected by the 13 state assemblies, and 44 are appointed by the king following the prime minister's recommendation. Representatives of the House are elected from single-member districts by universal adult suffrage. The 222 members of the House of Representatives are elected to parliamentary terms lasting up to 5 years. Legislative power is divided between federal and state legislatures.

The Malaysian legal system is based on English common law. The Federal Court reviews decisions referred from the Court of Appeal; it has original jurisdiction in constitutional matters and in disputes between states or between the federal government and a state. Peninsular Malaysia and the East Malaysian states of Sabah and Sarawak each have a high court.

Principal Government Officials
Prime Minister--Mohd Najib bin Abdul Razak
Foreign Minister--Anifah Aman
Ambassador to the U.S.--Jamaluddin Jarjis
Ambassador to the UN--Hamidon Ali

Malaysia maintains an embassy in the U.S. at 3516 International Court NW, Washington, DC 20008, tel. (202) 572-9700; a Consulate General at 550 South Hope Street, Suite 400, Los Angeles, CA 90071, tel. (213) 892-1238; and a Consulate General at 313 East 43rd Street, New York City, NY 10017, tel. (212) 490-2722/23.

Malaysia's predominant political party, the United Malays National Organization (UMNO), has held power in coalition with other parties continuously since independence in 1957. The UMNO coalition's share of the vote declined in national elections held in May 1969, after which riots broke out in Kuala Lumpur and elsewhere, mainly between Malays and ethnic Chinese. Several hundred people were killed or injured. The government declared a state of emergency and suspended all parliamentary activities.

In the years that followed, Malaysia undertook several initiatives that became integral parts of its socioeconomic model. The New Economic Policy (NEP), launched in 1971, contained a series of affirmative action policies designed to benefit Malays and certain indigenous groups (together known as Bumiputras or "sons of the soil"). The constitution was amended to limit dissent against the specially-protected and sensitive portions of the constitution pertaining to the social contract. The government identified intercommunal harmony as one of its official goals. The previous alliance of communally based parties was replaced with a broader coalition--the Barisan Nasional (BN) or National Front. The BN won large majorities in the 1974 federal and state elections.

Mahathir Mohamad was Prime Minister between 1981 and 2003, leading UMNO and BN to successive election victories. Mahathir emphasized economic development during his tenure, in particular the export sector, as well as large-scale infrastructure projects. Mahathir attributed the success of the Asian tiger economies to the "Asian values" of its people, which he believed were superior to those of the West. Mahathir sharply criticized the International Monetary Fund (IMF), international financiers, and Western governments during the economic and financial crisis that affected Asia in 1997-1998, and denied that the sharp downturn was due to economic or corporate mismanagement, corruption, or "crony capitalism."

The end of Mahathir's tenure was marred by a falling out with his deputy and presumed successor, Anwar Ibrahim. In September 1998, Mahathir dismissed Anwar and accused him of immoral and corrupt conduct. Although Anwar was convicted on both charges in 1999 and 2000, the trials were viewed as seriously flawed. Malaysia's Federal Court eventually freed Anwar after overturning his immoral conduct conviction in September 2004.

Mahathir stepped down as Prime Minister in October 2003 after 22 years in power, and his successor, Deputy Prime Minister Abdullah Ahmad Badawi, was sworn into office. Abdullah called elections and won an overwhelming victory in March 2004. Abdullah, an Islamic scholar, promoted the concept of "Islam Hadhari" or "civilizational Islam," emphasizing the importance of education, social harmony, and economic progress. His relationship with Mahathir eventually soured, with Mahathir expressing regret at supporting Abdullah to be his successor.

Malaysia held national elections in March 2008. UMNO and its coalition allies in the BN won a simple majority of the seats in the national parliament, but for the first time in history failed to gain the two-thirds majority necessary to amend the constitution. A loose coalition of opposition parties, called the Pakatan Rakyat or People's Alliance, led by Anwar Ibrahim, won 82 of 222 seats in parliament and took control of the state-level assemblies in five of Malaysia's 13 states. However, in February 2009 the opposition Alliance lost control of one of the states through defections of its assembly members--several members of the opposition and two from the BN became independent, bringing the opposition strength down to 79 members and the BN to 138 members. Prime Minister Abdullah, taking responsibility for his party’s poor showing in the March 2008 general election, stepped down as Prime Minister in a carefully timed transfer of power to his deputy, Mohd Najib bin Abdul Razak, in April 2009.

The Najib administration's cornerstone policy is the "1Malaysia" initiative, which emphasizes national unity amongst Malaysia's ethnically diverse population. Other initiatives include the Government Transformation Program to improve government services delivery systems; the Economic Transformation Program to provide a framework to emphasize private investment and de-emphasize public investment; and the New Economic Model (NEM), to reform the 1970s (and still current) economic policy known as the New Economic Policy.

Since it became independent in 1957; Malaysia's economic record has been one of Asia's best. Real gross domestic product (GDP) grew by an average of 6.5% per year from 1957 to 2005. Performance peaked in the early 1980s through the mid-1990s, as the economy experienced sustained rapid growth averaging almost 8% annually. High levels of foreign and domestic private investment played a significant role as the economy diversified and modernized. Once heavily dependent on primary products such as rubber and tin, Malaysia today is a middle-income country with a multi-sector economy based on services and manufacturing. Malaysia is one of the world's largest exporters of semiconductor devices, electrical goods, solar panels, and information and communication technology (ICT) products.

Malaysia struggled economically during the 1997-1998 Asian financial crisis and applied several valuable lessons to its economic management strategies that contributed to the economy’s resilience to the 2008-2009 global financial crisis. GDP contracted 1.7% in 2009 compared to 4.6% growth in 2008, but has since rebounded, and is expected to be around 7% in 2010. Malaysian banks are well capitalized, conservatively managed, and had no measurable exposure to the U.S. sub-prime market. The central bank maintains a conservative regulatory environment, having prohibited some of the riskier assets in vogue elsewhere. Malaysia maintains high levels of foreign exchange reserves and has relatively little external debt.

The government continues to actively manage the economy with state-owned enterprises heavily involved in the oil and gas, plantation, ship building, steel, telecommunications, utilities, automotive, mining, and other sectors. Since 1971, ethnic preferences have been given to Bumiputras (ethnic Malays and indigenous peoples) by requiring 30% Bumiputra ownership in new businesses. Prime Minister Najib’s New Economic Model reform program includes changes to modify these ethnic preferences and to divest state enterprises while increasing the private sector’s role in stimulating higher levels of investment and boosting GDP growth. The NEM aims to create a business environment more conducive to long-term sustained economic growth, development, and investment, with the goal of Malaysia becoming a high-income, developed nation by 2020.

Malaysia has a managed float currency exchange regime. It gives flexibility for the ringgit to adjust to global economic and financial developments and has accorded a level of stability against the currencies of Malaysia’s major trading partners.

Regional cooperation is a cornerstone of Malaysia's foreign policy. It was a founding member of the Association of Southeast Asian Nations (ASEAN).

Malaysia is an active member of the Asia Pacific Economic Cooperation (APEC) forum, the Organization of the Islamic Conference (OIC), the Non-Aligned Movement (NAM), and the United Nations.

Malaysia is a frequent contributor to UN and other peacekeeping and stabilization missions, including recent deployments to Lebanon, Timor-Leste, Philippines, Indonesia, Pakistan, Sierra Leone, Sudan, Western Sahara, Nepal, and Kosovo.

The United States and Malaysia share a diverse and expanding partnership. Economic ties are robust. The United States is Malaysia's third-largest trading partner and Malaysia is the eighteenth-largest trading partner of the United States. Annual two-way trade amounts to $33 billion. In October 2010 Malaysia joined negotiations for a Trans-Pacific Partnership free trade agreement.

The United States is the largest foreign investor in Malaysia on a cumulative basis, and was the largest source of new foreign direct investment in Malayia in 2010. American companies are particularly active in the electronics, manufacturing, and oil and gas sectors. According to Malaysian data, U.S. direct investment in the manufacturing sector in Malaysia as of year-end 2009 was $15.1 billion, with billions of dollars in additional investment in the oil and gas and financial services sectors of the economy.

The United States and Malaysia cooperate closely on security matters, including counterterrorism, maritime domain awareness, and regional stability. The relationship between the U.S. and Malaysian militaries is also strong with numerous exchanges, training, joint exercises, and visits. The U.S. and Malaysia signed a Mutual Legal Assistance Treaty (MLAT) in July 2006 during the visit to Kuala Lumpur by Secretary of State Condoleezza Rice.

The United States and Malaysia have a long history of people-to-people exchanges. Well over 100,000 Malaysians have studied in the U.S. At any one time there are over 7,000 Malaysians studying at U.S. universities. Last year approximately 130 Malaysians took part in U.S. Government-sponsored exchange programs for professional development and study. Each year, about 50 Americans travel to Malaysia under U.S. Government auspices to share their experience as visiting academics or speakers. In November 2010, the U.S. and Malaysia signed a bilateral Memorandum of Understanding on Science and Technology Cooperation.

There are approximately 1,500 alumni of the International Visitor Leadership Program (IVLP) and 2,000 from the Fulbright, Humphrey, Eisenhower, and Youth Exchange for Study (YES) programs. Prominent Malaysian alumni include federal ministers, deputy ministers, and members of parliament from both the ruling party and opposition parties. At least four current and past chief ministers (state governors) are alumni, and former Prime Minister Mahathir is an alumnus of a 1973 program. These alumni have used their educations to create a stronger Malaysian society and have built enduring understanding between Malaysia and America. Their contributions to Malaysian society will continue for many years to come.

Principal U.S. Embassy Officials
Ambassador--Paul W. Jones
Deputy Chief of Mission--Robert G. Rapson
Political Counselor--Brian D. McFeeters
Economic Counselor--Paul A. Brown
Commercial Counselor--Nasir A. Abbasi
Public Affairs Officer--Scott M. Rauland
Agricultural Attache--David W. Cottrell
Consul General--Charles J. Wintheiser

[This is a mobile copy of Malaysia (01/28/11)]

Short URL: http://m.state.gov/md169533.htm


Heilbrunn Timeline of Art History

Europe and the Islamic World, 1600–1800

Thematic Essays

By Category

By Geographical Region & Time Period
By Department

At the beginning of this period, the European presence in the Islamic world was largely based on trade. Dutch, French, English, and Portuguese merchants first arrived in the late fifteenth century, attracted by the wealth that could be acquired in exporting luxury items to the European market, and encouraged by the Mughal and Safavid governments, which desired trade partners to stimulate the economy. Diplomatic ties later officially cemented these partnerships. The first British representatives arrived in Persia in 1622 and the French in 1638. The Portuguese landed in India in 1498 and the French soon afterward, but the British, under the aegis of the East India Company, would prove to be the chief force in the subcontinent. Sir Thomas Roe brokered the first trade treaty in 1615. The Ottoman empire was initially more isolated as it had a strong domestic trade network, but in the eighteenth century it began to receive European merchants and consuls as well as to send out its own. One mission from Turkey visited the court of Louis XV of France in the 1720s.

As the Europeans were introduced to many new kinds of textiles, carpets, spices, and clothing, so too was the Islamic world enriched.

As the Europeans were introduced to many new kinds of textiles, carpets, spices, and clothing, so too was the Islamic world enriched. European art circulating among court artists transformed painting under both the Mughals and the Safavids. By carefully copying the engravings in sixteenth-century illustrated Bibles presented by Jesuit missionaries, Indian artists learned techniques of modeling and spatial recession that they then applied to their own works. Illustrations in books of herbals affected the way flowers and plants were depicted. In Persia, oil paintings had a greater effect, the lifesize portraits of Louis XIV sent to Isfahan eventually metamorphosing into Zand and Qajar state portraits. Although manuscripts such as the Bellini Album ( attest that European drawings were known in Turkey, it was exposure to the French Baroque that captured the local imagination. Soon after the return of travelers to Versailles, flamboyant architectural ornament began to appear on both royal residential buildings and mosques.

By the end of the period, European colonial interests had upset this equitable cultural exchange. The British East India Company established an army to protect its commercial interests in India; its 1757 defeat of the nawab of Bengal led to further armed conflicts and finally to the 1858 declaration of British sovereignty over the country. The British also became involved in interdynastic conflicts in the Arabian Peninsula and established a military post in Muscat, Oman. Napoleon invaded Egypt in 1798, and though he was forced to withdraw from the area in 1801, the French would later occupy parts of North Africa. The Dutch became involved in lands further east, especially in the Indonesian archipelago, where islands controlled by different Muslim rulers were united as one colony.

Marika Sardar
Institute of Fine Arts, New York University


Beatriz Gomez hails from Venezuela, where rather than playing with fancy toys, she spent her time paying attention to the little things in life. She says the time she had to enjoy the world around her plays a part in all of her paintings, sculptures, collages and murals.

Gomez's mentor was an apprentice to Frida Kahlo and Diego Rivera, Mexico's most famous artist couple. A picture of Kahlo and Rivera hang in the sunroom of Gomez's home.

"[My mentor] is one of my inspirations because she was in an accident in her life and she kept going with so many troubles, to walk and to be alive, but she did it," Gomez said.

Gomez's resume includes stage and costume design for international performing artists like Christina Aguilera, Santana and Sting. Many of them now own her artwork.

Gomez is currently a resident artist at the Denver Art Museum, where she mentors children who want to learn more about art and is a regular contributor to CelebrARTE, the Museum's monthly bilingual art program. CelebrARTE highlights the rich heritage of Latinos around the world through interactive family activities.

In her classes, Gomez teaches that art really does imitate life.

"Nothing is a mistake. You might think, 'Oh no, that came out wrong' or 'That doesn't look good,' but you can transform it into something else. There is a reason it turned out that way, and since there is nothing planned, whatever happens is okay," she said.

Hispanic Heritage month lasts through mid-October, and you can check back every Monday for more interesting stories from the Latino community.

For more information, visit: www.beatrizgomez.com

Alexis Bridenbaugh contributed to the report


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